Soil properties, presence of microorganisms, application dose, soil moisture and temperature influence the degradation rate of Allyl isothiocyanate in soil

Chemosphere 244 (2020) 125540

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Soil properties, presence of microorganisms, application dose, soil moisture and temperature influence the degradation rate of Allyl isothiocyanate in soil Jie Liu a, Xianli Wang b, Wensheng Fang a, Dongdong Yan a, Dawei Han a, Bin Huang a, Yi Zhang a, Yuan Li a, Canbin Ouyang a, Aocheng Cao a, Qiuxia Wang a, * a

State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China Institute for Agri-food Standards and Testing Technology, Shanghai Academy of Agricultural Science, Shanghai, 201106, China

b

h i g h l i g h t s

g r a p h i c a l a b s t r a c t


Soil texture and environmental factors affect the AITC degradation.
Orthogonal design establishes the extraction method of AITC in soil.
AITC degradation depends on soil characteristics and application rate.
Microbial degradation is the main pathway for AITC degradation in soil.
AITC degradation generally accelerates with increasing temperature and humidity.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 July 2019 Received in revised form 1 December 2019 Accepted 2 December 2019 Available online 3 December 2019

Allyl isothiocyanate (AITC) is a soil fumigant derived from plants that can effectively control soil-borne diseases. Fully understanding the impact of various factors on its degradation can contribute to its effectiveness against pests and diseases. First, orthogonal design determined the extraction method of AITC in soil, that is using ethyl acetate as the extraction reagent, vortexing for 1 min as the extraction method and holding for 30 min as the method time. Then we studied the effects of soil texture and environmental factors on the rate and extent of AITC degradation in soil. The half-lives of nine origins soils varied from 12.2 to 71.8 h that were affected by the soil’s electrical conductivity, available nitrogen, pH and organic matter content. Biotic degradation of AITC contributed significantly (68%e90%) of the total AITC degradation in six soil types. The degradation rate of AITC decreased as the initial dose of AITC increased. The degradation rate of AITC in Suihua soil generally increased with increasing temperature and soil moisture. The effect of temperature on AITC degradation was more pronounced when the soil was moist, which has practical implications for the control of soil pests and diseases. In agricultural soil, the soil’s characteristics and environmental factors should be considered when determining the appropriate AITC dose suitable for soil borne disease while at the same time minimizing emissions and impact on the environment. © 2019 Elsevier Ltd. All rights reserved.

Handling Editor: T Cutright Keywords: Allyl isothiocyanate Soil Half-life Biotic degradation Environmental factors Soil characteristics

1. Introduction * Corresponding author. E-mail address: [email protected] (Q. Wang). https://doi.org/10.1016/j.chemosphere.2019.125540 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

China has always been the world’s largest vegetable producer

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J. Liu et al. / Chemosphere 244 (2020) 125540

and consumer; it’s planting area of vegetables is second only to food crops and has become an important pillar industry for agricultural economic development (NDRC, 2012). By the end of 2017, Chinese vegetable yield reached 181,905,644.9 tons (FAOSTAT, 2017). However, one of the main factors affecting the yield and quality of high value-added crops is the spread of soil diseases, and soil fumigation is recognized as the most direct and effective way to control these problems presented in the soil (Cao et al., 2017). In the past, methyl bromide (MB) was the most widely used soil fumigant globally as it was effective against soil-borne pathogens, pests, nematodes and weeds (Taylor, 1994; Ruzo, 2006). However, MB was banned globally under the Montreal Protocol in 2015 because of its ozone-depleting properties (UNEP, 2015). Hence, farmers are looking for efficient and safe alternatives to MBdAllyl isothiocyanate (AITC) is one of them. AITC is a natural, sulfur-containing secondary metabolite and the main component of isothiocyanate substances and is predominantly found in cruciferous vegetables such as horseradish, mustard and wasabi (Chin and Lindsay, 1993; Chen and Ho, 1998). Its precursor ‘sinigrin’ is located in plant vacuoles (Fenwick et al. 1983). When the plant membrane is disrupted, myrosinase decomposes sinigrin to produce AITC and other substances. The chemical structure of AITC is shown in the Figure A1. AITC can inhibit the growth of microorganisms by changing the structure of proteins. Specifically, the AITC cleaved the disulfide bond of the cystine portion, and then formed a polymer. In addition, AITC can attack the free amino groups of lysine and arginine residues, and then form thiourea-like derivatives (Kawakishi and Kaneko, 1985, 1987). It has been reported that AITC can effectively control nematodes (Zasada and Ferris, 2003), bacteria, various pathogenic fungi (Dhingra et al., 2004; Wu et al., 2011) as well as prevent weed seeds germination (Bangarwa et al., 2011). At a lower concentration (0.1e2.0 mg L1), AITC can significantly inhibited the spore germination and mycelium growth of candida (Bla zevi c et al., 2019). What’s more, it can significantly increase the marketable yield of the crop without reducing the quality of the crop fruit (Ren et al., 2018). AITC’s degradation behavior in soil will affect its ability to inhibit microorganisms. The characteristics of the soil and the environmental conditions are considered to be the main two factors that will influence the AITC degradation. Han et al. (2018) reported that the degradation rate of fumigants was significantly different in ten different types of soil; and Qin et al. (2016) confirmed that the degradation half-life of fumigants in coarse soil was faster than in finer soil. Meanwhile, the degradation of fumigants is mainly dependent on microorganisms (Ma et al., 2001), whose distribution in soil is influenced by temperature, humidity and the application

rate of the fumigant to the soil (Gan et al., 1999). Our study aimed to examine the key factors that influence the degradation of AITC in soil including (1) the effects of the soil’s characteristics and different environmental factors on the rate of AITC degradation and (2) the dose of AITC and the influence of microorganisms, temperature and moisture on AITC degradation. For this purpose, an optimized method to detect and measure AITC residues in the soil was developed. Understanding the influence of these factors on the degradation rate of AITC will help farmers to optimize the use of this fumigant for controlling pests and diseases. 2. Material and methods 2.1. Optimization of the extraction method for measuring AITC residues in soil 2.1.1. Soils and chemicals Beijing Shunyi soil was collected from 10 to 20 cm below the surface of agricultural fields. It was then air-dried and sieved through a 2 mm mesh. Deionized water was used to adjust the soil moisture content to 12% prior to storing it in a sealed bag for later use. The characteristics of Shunyi soil are shown in Table 1a. AITC with an analytical purity (>98%) was obtained from SigmaAldrich Corporation (St Louis, USA). Analytical grade ethyl acetate (99.7% purity) and anhydrous sodium sulphate were provided by Beihua Fine-Chemicals Co. Ltd. (Beijing, China) and Sinopharm Chemical Reagent Co. Ltd. (Beijing, China), respectively. 2.1.2. Treatment of soil with AITC and extraction of AITC Twenty microliters of 2 g L1 AITC solution were added to 8.0 g of soil contained in a 20 mL vial, and replicated three times. Each vial was quickly sealed with an aluminum cap with a Teflon-faced butyl rubber septum, inverted and shaken several times to ensure that the AITC was thoroughly mixed with the soil. Each vial was uncapped to allow anhydrous sodium sulphate at a water/Na2SO4 ratio of 1:7 and 8 mL of extraction reagent to be added (Borek et al., 1995). The vials were resealed and vortexed at a high speed of 2500 rpm for 1 min. The concentration of AITC was measured by using 0.22 mm nylon syringe to withdraw filtered supernatant from each vial and injecting 1e1.5 mL into a GCMS-QP2010 SE gas chromatograph equipped with mass spectrophotometer (Shimadzu, Japan) operated in electron ionization mode and quantified in selected ion monitoring (SIM) mode. The Gas Chromatograph conditions were: A Restek® Rtx-5MS GC column (Chrom Tech Inc, USA) 30.0 m  0.25 mm  0.25 mm was used for separation of the injected components. Carrier gas (He) flow rate and inlet

Table 1a Origin, region, texture and physicochemical properties of soil samples used in this study. Soil origin

Region

Sand

Clay

Silt

Texturea

dddd %ddd Anqiu (36 280 41.4500 N 119 120 43.4900 E) Chifeng (42 150 23.9200 N 118 520 57.8700 E) Dazhou (31 120 38.8400 N 107 270 47.7200 E) Miyun (40 220 30.2100 N 116 500 13.6000 E) Shunyi (40 070 44.4900 N 116 380 56.0000 E) Suihua (46 390 2.0700 N 126 570 46.8900 E) Wenshan (23 220 14.3000 N 104 140 33.3500 E) Yangling (34 150 8.5000 N 108 060 16.3600 E) Yongzhou (26 250 26.1400 N 111 360 25.2200 E)

Shandong Neimeng Sichuan Beijing Beijing Dongbei Yunnan Shanxi Hunan

25 60 70 58 75 75 73 74 36

10 35 16 36 13 17 19 18 22

65 5 14 6 12 8 8 8 42

silt loam soil sandy clay soil sandy loam soil sandy clay soil sandy loam soil sandy loam soil sandy loam soil sandy loam soil loam soil

OM

EC

pH

ddmg kg1 dd

AN

K

g kg-1

us/cm

1:2.5

132 25 37 130 100 59 70 23 50

15 14 43 21 24 67 63 18 15

843 173 220 861 143 378 335 205 86

6.1 7.6 5.2 6.6 7.4 6.7 4.2 7.7 5.3

513 361 278 502 483 839 203 329 239

Note. pH and EC were measured with soil to deionized water at a ratio of 1:2.5; AN: available nitrogen; K: rapidly available K; OM: organic matter; EC: electrical conductivity; P: available phosphorus. a The texture of soil was classified according to the United States Department of Agriculture (USDA) textural soil classification system.

J. Liu et al. / Chemosphere 244 (2020) 125540

temperature were set at 1.0 mL min1 and 250  C. The oven temperature program was initially set at 60  C, increasing to 100  C at 10  C min1 and held for 2 min. The Mass Spectrometer conditions were as followed: ion source temperature and transfer line temperature were both 230  C. The qualifier ions were determined to be 72 m/z and 99 m/z, and the quantitation ion is 99 m/z. 2.1.3. Experimental design The interaction between the extraction parameters resulted in the selection of an orthogonal design L27 (313) to study three factors: extraction reagent (A), extraction time (B) and extraction method (C). Three levels of each factor were selected. The effect of these three factors and their interactions were examined through one-way analysis of variance using SPSS statistical software. These factors and the experimental layout are shown in Tables A1 and A2 2.2. Factors influencing the AITC degradation in soils 2.2.1. Soil description and sample preparation Agricultural soils from nine regions that had not applied the AITC were collected during the same season (early summer). Five sites of cultivated layer (10e20 cm) soil were randomly selected from each plot, and all soil samples were evenly mixed together then mixed all soil samples evenly together. Soils were sieved into a 2 mm particle size to remove clods and plant residues and then stored in sealed plastic buckets at room temperature. According to the United States Department of Agriculture (USDA) textural soil classification system, these nine soils are classified into four types (silt loam soil, sandy loam soil, sandy clay soil, loam soil) and crops planted in nine agricultural fields are ginger (Anqiu), corn (Chifeng), konjac (Dazhou), tomato (Miyun), strawberry (Shunyi), corn (Suihua), Panax Notoginseng (Wenshan), wheat (Yangling) and lily (Yongzhou). The soil detailed information was given in Tables 1a and 1b. AITC was added to these soils as described in 2.1. Twenty microliters of ethyl acetate solution containing 8 g L1 AITC was added to 8 g of soil contained (dry weight equivalent) in a 20 mL headspace vial and sealed. Vials were placed into a constant temperature incubator at 28  C. After about 2, 6, 8, 12, 24, 48, 72, 120, 240, 336, 504, 840 h of incubation, triplicate samples from each treatment were refrigerated at 80  C to prevent degradation. The extract solution was quantified by the analytical method described in 2.1. The orthogonal design was used to statistically analyze the influence of the extraction method, as described in 2.1.

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the vials were 20 mL from these solutions. Only Suihua, Yongzhou and Miyun soils were used in this experiment. Their water content was adjusted to 12% and the AITC was added to each soil type to give equivalent doses of 20, 50 or 100 mg g1. The bags were sealed, incubated at 28  C for 2, 6, 12, 24, 48, 72, 120, 240 and 408 h and then refrigerated 80  C for later AITC extraction and quantification. 2.2.4. Effect of soil moisture Suihua soil samples were adjusted to 3, 6, 12, 18 or 30% (w/w) water content using deionized water. Each sample was mixed evenly and packed into sealed bags for 24 h to homogenize the soil moisture content. The dosage of AITC was kept constant across all the soils at 20 mg g1. Twenty microliters of ethyl acetate solution containing 8 g L1 AITC was added to each soil sample and incubated at 28  C for 2, 6, 8, 12, 24, 48, 72, 120, 240 h and then refrigerated at 80  C for later AITC extraction and quantification. 2.2.5. Effect of temperature Suihua soil samples with of 3, 6, 12, 18 or 30% water content were incubated at 4, 18, 28, 38 or 48  C in the dark to determine the effect of temperature and humidity on the degradation of AITC. The dosage of AITC was kept constant across all the soils at 20 mg g1. Twenty microliters of ethyl acetate solution containing 8 g L1 AITC was added to each soil sample and incubated at 28  C for 2, 6, 8, 12, 24, 48, 72, 120, 240 h and then refrigerated at 80  C for later AITC extraction and quantification. 2.3. Data analysis and statistics The added recovery rate of AITC was calculated as:

R ¼ ðCe  Cb Þ = Ca  100% where R is recovery rate (%), Ce is the extraction amount of AITC in soil (mg kg1), Cb is the amount in blank samples (mg kg1), Ca is the amount of AITC added to the soil (mg kg1). First-order regression is well described for the results from degradation of AITC (Hanschen et al., 2015):

Ct ¼ C0 exp

ðktÞ

where (Ct) is the concentration at a certain time (t), (C0) is the concentration at the time zero (t ¼ 0), k is the first-order rate constant (d1), and t1/2 is the half-life period which can be calculated as—

2.2.2. Effect of soil microorganisms AITC could be degraded by a combination of chemical and biological processes. To determine the significance of each process, Suihua, Miyun, Chifeng, Yangling, Yongzhou and Wenshan soils were selected according to the highest and lowest values of some physical and chemical indicators which were available nitrogen, electrical conductivity and pH, respectively. (Table 1a). Then they were divided into two parts: one was sterilized and the other was left unsterilized. Each soil was sterilized by autoclaving them at 121  C for 30 min twice in succession and adjusted to 12% water content. The dosage of AITC was kept constant across all the soils at 20 mg g1. Twenty microliters of ethyl acetate solution containing 8 g L1 AITC was added to each soil sample and incubated at 28  C for 2, 12, 24, 72, 120, 240, 408, 576, 744 h and then refrigerated at 80  C for later AITC extraction and quantification.

Biodegradationð%Þ ¼ 1  Chemical degradationð%Þ

2.2.3. Effect of AITC doses and soil origin The AITC doses used were 20, 50 or 100 mg g1. In order to eliminate the effect of different concentrations of solvent 8, 20 and 40 g L1 solutions of AITC were used. All doses added to the soil in

where ksoil is the AITC degradation rate constant for a non-sterile soil, kchemical is the chemical rate constant for chemical AITC degradation, and kbiological is the biological rate constant for microbial AITC degradation (Qin et al., 2016; Han et al., 2018).

t1=2 ¼ lnð2Þ = k Degradation in non-sterile soils was assumed to be both chemical and biological, but only chemical in sterilized soils. The difference in degradation rate between them was considered to be due to microbial degradation (Gan et al., 1999). The degradation of AITC in non-sterile soil therefore:

ksoil ¼ kchemical þ kbiological Chemical degradationð%Þ ¼ kchemical = ksoil  100

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J. Liu et al. / Chemosphere 244 (2020) 125540

OriginPro 8.0 software was used to fitted the degradation model (OriginLab Corporation, USA). One-way ANOVA for orthogonal design and Duncan’s multiple range test were performed by SPSS v22.0 statistical software (SPSS Inc, Chicago, IL, USA) to acquire the significance of differences between means obtained under the treatments at the 5% level of significance. Similarly, multiple comparison test and Pearson correlation coefficient were calculated by SPSS. 3. Results and discussion 3.1. Optimization of AITC extraction Twenty-seven experiments in an orthogonal design were carried out to identify the optimal conditions for AITC extraction from soil (Table A2). K1, K2 and K3 were the average recovery rates of AITC under the various conditions that examined factor A (extraction reagent), factor B (extraction time) and factor C (extraction method) and their combinations. The influence factor to the extraction yield followed the order A > C > B. Factor A, factor B, factor C and factor A*C were statistically significant at P < 0.05 according to the ANOVA test (Table A3). There were no statistical differences observed between factors A  B and factor B  C. The factors that influenced the extraction of AITC declined in sequential order were: A > A  C > B > C > A  B > B  C. Since there was an interaction between factor A and factor C, we determined the optimal combination by multiple comparisons. The results of multiple comparison test were shown in Table A4. It can be seen from the table that the first combination is optimal (98%), that is, A1  C1. According to our results, the optimal conditions were A1, C1 and B1 which used ethyl acetate (A1; extraction reagent), vortex for 1 min and static (C1; extraction condition) 30 min (B1; extraction time) to extract AITC from soil. 3.2. Effects of soil origin on AITC degradation The degradation rate constant (k), half-life (t1/2), and correlation coefficient (r2) of different types of soil are shown in Table 1b. The correlation coefficient (r2) ranging from 0.89 to 0.98 which indicated the first-order kinetics model was a good fit to the AITC degradation data. Meanwhile the half-life of AITC ranged from 12.2 to 71.8 h in the nine tested soils indicating that AITC degradation rate was affected by soil origin. Among them, the fastest degradation rate is Yangling soil, and the slowest degradation is Anqiu soil. Similar experimental results were also reported by Borek et al. (1995) who showed the half-lives of AITC in six soils were 20e60 h. The relationship between a soil’s physicochemical properties

Table 1b The degradation parameters of AITC in these soils producing high-value crops in nine regions throughout China. Soil origin (crop)

k±SE (h1)

t1/2(h)

r2

Anqiu (ginger) Chifeng (corn) Dazhou (konjac) Miyun (tomato) Shunyi (strawberry) Suihua (corn) Wenshan (Panax Notoginseng) Yangling (wheat) Yongzhou (lily)

0.0097 ± 0.001 g 0.040 ± 0.003 c 0.032 ± 0.004 d 0.018 ± 0.0005 f 0.047 ± 0.002 b 0.037 ± 0.001 c 0.030 ± 0.0008 e 0.057 ± 0.004 a 0.030 ± 0.004 g

71.8 17.3 21.6 38.8 14.8 18.7 29.7 12.2 23.8

0.92 0.98 0.96 0.98 0.98 0.95 0.89 0.97 0.92

Regression curves were produced by using first-order kinetics. k (h1)，t1/2 (h) and r2 represent degradation rate. Constant, half-life and correlation coefficient, respectively. Values are means ± SD (n ¼ 3). According to the Duncan’s multiple range test, different letters in the same column indicate significant differences between treatments (p < 0.05).

and the half-life of AITC were also determined by the Pearson correlation coefficient (r). These results showed an extremely significant positive correlation between AITC half-life and electrical conductivity (EC) (r ¼ 0.827). As EC increased carbon dioxide in the soil decreased, which suggested that EC inhibited soil respiration (Setia et al., 2011). Soil conductivity is an indicator of water-soluble salts in the soil. Rietz (2003) suggested that salt inhibited the growth and activity of soil microbes by affecting the osmotic pressure in the microbial cell walls, and that an increase in salinity created osmotic stress which affected their growth and activity. Therefore, soils with high EC may inhibit the growth and activity of AITC-degrading bacteria leading to increased concentrations of AITC. The Pearson correlation coefficient between the available nitrogen (AN) and the AITC half-life was 0.74, indicating a strong positive correlation between them. This suggests that the increased concentrations of AN slow the degradation rate of AITC. Previous study has shown that increasing nitrogen will alter the soil’s microbial community structure (Fierer et al., 2012). However, Borek et al. (1995) showed a different result that the half-life of AITC and AN were negatively correlated. The nitrogen measured by Borek was total nitrogen that included all forms of inorganic and organic soil nitrogen (Rutherford et al., 2007). Organic nitrogen accounts for a large proportion of total nitrogen in the soil, and an increase in organic nitrogen content would enrich the microbial population, promote its activity and population size (Geisseler et al., 2010). Therefore, the higher total nitrogen that soil contents, the more available microbial communities are used to degrade AITC. However, the nitrogen content measured in our research was the available nitrogen, which included ammonium nitrogen and nitrate nitrogen that belong to inorganic nitrogen. On the other hand, previous study noted a high and positive correlation between inorganic nitrogen concentration and conductivity, indicating that the production of inorganic nitrogen will increase conductivity nchez-Monedero et al., 2001). Therefore, soil conductivity in(Sa creases as the available nitrogen increases and excessive conductivity will discourage microorganism survival, thereby slowing down the degradation rate of AITC. There was a weakly negative correlation between AITC half-life and soil pH (r ¼ 0.302). Soil pH influences the rate of pesticide degradation which in turn influences the chemical degradation of organic matter and the survival of microbial communities. In our research, soils from Chifeng, Shunyi and Yangling have pH values of 7.59 (t1/2 ¼ 17.3 h), 7.42 (t1/2 ¼ 14.8 h) and 7.67 (t1/2 ¼ 12.2 h), respectively, which have a faster degradation rate than other neutral or mildly acidic soils. Previous research showed that AITC degradation was inhibited in acidic solutions and degraded slowly in alkaline solutions (Ohta et al., 1995; Tsao et al., 2000). It was decomposed by a nucleophilic attack of water against its isothiocyanate group (-N]C]S). In aqueous solution, hydroxyl ions are added to the carbon atom of eN]C]S to form monothiocarbamates, which is irreversible association (Patai, 2010). Pechacek et al. (1997) showed that in three aqueous solutions with a pH of 4, 6 or 8, the main decomposition product of AITC, allylamine, was highest in an alkaline solution. Meanwhile, soil pH affects microbial community diversity, as there is a positive correlation between bacterial community abundance, bacterial diversity and pH (Fierer and Jackson, 2006). At pH 4 to 8, bacterial diversity is nearly doubled (Fierer and Jackson, 2006; Rousk et al., 2010). We theorize that the degradation rate of AITC is faster in alkaline than acidic soil because alkaline soil best supports the survival of AITC-degrading bacteria. AITC half-life was negatively correlated with OM content in the

J. Liu et al. / Chemosphere 244 (2020) 125540

soil, but this correlation was not significant (r ¼ 0.195). Borek et al. (1995) showed that AITC degraded faster in soils with high OM content, possibly due to the reaction of isothiocyanate functional group with nucleophilic groups present in organic matter. Gimsing et al. (2009) reported that OM is the primary sorbent of isothiocyanate in soil. A high OM content will increase and enrich the microbial flora in the soil. Wu et al. (2011) proved that high OM content contributed to a large microbial population that accelerated the degradation of pesticide in soil. In our research, Suihua soil had the highest OM content and its degradation half-life was 18.7 h. However, the degradation half-life of AITC in Chifeng soil and Yongzhou soil that both had very low OM content was similar to that of Suihua soil. This suggested that the degradation of AITC in soil was determined not only by OM alone, but also by a combination of factors. The degradation of AITC in soil is a complex process. Based on our comprehensive analysis of the data on degradation rate of AITC in nine origins soils, we conclude that AITC degradation is affected by many different physical and chemical properties and microbial activity in soil that collectively contribute to its degradation.

3.3. Effects of soil microorganisms on AITC degradation in soil The AITC degradation data were a good fit (r2 values mostly greater than 0.91) to first-order kinetics in six origins of sterilized and unsterilized soil (Table 2). Sterilizing the soil resulted in a significant decrease in the degradation rate of AITC. The amount of AITC in the sterilized soil was significantly greater than that in the non-sterilized soil. The AITC half-life values in sterilized Chifeng, Shunyi, Suihua, Yangling, Yongzhou and Wenshan soils were 6.72, 3.12, 9.77, 3.16, 3.0 and 4.49 times longer than that in the unsterilized soil samples of the same, respectively. The degradation rate of AITC in sterilized soil was slower than in unsterilized soil. The contribution of biodegradation to the total degradation of AITC in these soils was 85.00%, 68.09%, 89.73%, 68.42%, 67.67% and 82.67%, respectively (Table 2). The results demonstrate both biological and chemical mechanisms contributed to the degradation of AITC, but microbial degradation was probably the most important pathway. Correlation analysis between physicochemical properties and degradation rate of sterilized soil showed that they were no correlation between them. This indicates that AN, EC and pH may mainly affect the activity of microorganisms in soil, thus affecting the degradation rate of AITC, but there may be another unexplored factor that affects chemical degradation, which requires continued exploration in future experiments. The presence of pesticide-degrading microbes, available nutrients and many other environmental factors may affect the overall pesticide biodegradation rate (Aislabie and Lloyd-Jones, 1995). The soil is a complex environment with many different kinds of

5

microorganisms, each containing different functional enzymes (Caldwell, 2005). When organic substances enter the soil, they will biodegrade them according to the available degrading enzymes contained by microbes. Fewson (1988) showed that bacteria or their functional enzymes transport pesticides and their metabolites into bacterial cells for degradation. Therefore, the persistence of AITC in the soil is influenced by microbial abundance and activity.

3.4. Effects of dose on AITC degradation rate in soil The AITC degradation data were a good fit (r2 values 0.93e0.98) to first-order kinetics when AITC doses of 20, 50 and 100 mg g1 were applied to the Shunyi, Suihua and Yongshou soils (Table 3). The degradation rate constant (k) decreased in most cases as the dose rate increased. In addition, the half-life values of AITC in each of the soil were longer as the dose increased. Specifically, in the three soils, the degradation half-life of AITC was all expressed as t1/2 (100 mg g1) > t1/2 (50 mg g1)> t1/2 (20 mg g1), which indicates that the degradation of AITC in soil is affected by the application rate. Pearson correlation analysis was carried out on the physical and chemical properties of soil and the degradation rate of three soils at three doses. The significance level was over 0.05, that is, there was no correlation between the physical and chemical indicators of the soil and the applied doses, and then analyzed the correlation between soil texture and dose and found to have only a significant negative correlation between the clay ratio and the medium dose (r ¼ 0.99). Some reports showed that the biomass activity of clay in the same proportion was much lower than that of sand and loam (Hassink, 1994; Colman and Schimel, 2013). Low biomass activity may cause AITC degradation rate to slow down. Duncan’s multiple range test of the AITC degradation rate in these three soils at different doses showed significant differences between AITC doses of 20 or 50 and 100 mg g1 applied to Yongzhou soil, while the difference of degradation rate in the medium and low doses of Shunyi and Suihua soil was not significant. Fierer and Jackson (2006) demonstrated that the diversity of bacterial community was the most abundant in pH neutral soil, but the lowest in acid soil. Therefore, under the same culture conditions, the difference in degradation rate may be due to differences in microbial activity (the pH of Shunyi, Suihua and Yongzhou soils were 7.4, 6,7 and 5,3, respectively.). A high application rate such as 100 mg g1 may inhibit the activity and diversity of AITC-degrading bacteria. Han et al. (2018) reported that Dimethyl Disulfide (DMDS) degradation rate at the lowest application dose was 8 times faster than the highest dose, and that there were differences in bacterial diversity after fumigation with different doses of DMDS. Although these differences were not significant they tended to show diversity at the phylum and genus levels. For example, Bacillus bacteria known to degrade pesticides were more abundant in soil exposed to low doses of

Table 2 Degradation parameters and biodegradation percentage of AITC in six different soils fumigated with an AITC doses of 20 mg g1 Soils

Chifeng Shunyi Suihua Wenshan Yangling Yongzhou

Sterilized soil

Unsterilized soil

k±SE (h1)

t1/2(h)

r2

k±SE (h1)

0.0060 ± 0.0008 a 0.015 ± 0.0001 e 0.0038 ± 0.0003 c 0.0052 ± 0.0001 cd 0.18 ± 0.0006 b 0.0097 ± 0.0002 de

116.3 46.2 182.7 133.3 38.5 71.5

0.91 0.87 0.98 0.93 0.94 0.94

0.040 0.047 0.037 0.030 0.057 0.030

± ± ± ± ± ±

0.003 c 0.002 b 0.001 c 0.0008 e 0.004 a 0.004 d

Biodegradation (%) t1/2(h)

r2

17.3 14.8 18.7 29.7 12.2 23.8

0.98 0.99 0.81 0.94 0.97 0.92

85.0 68.1 89.7 82.7 68.4 67.7

Regression curves were produced by using first-order kinetics. k (h-1)，t1/2 (h) and r2 represent degradation rate. Constant, half-life and correlation coefficient, respectively. Values are means ± SD (n ¼ 3). According to the Duncan’s multiple range test, different letters in the same column indicate significant differences between treatments (p < 0.05).

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J. Liu et al. / Chemosphere 244 (2020) 125540

Table 3 Degradation parameters of AITC at different application doses of AITC in three soils Doses

Shunyi

1

20 mg g 50 mg g1 100 mg g1

Suihua

Yongzhou

k±SE (h1)

t1/2 (h

r2

k±SE (h1)

t1/2 (h)

r2

k±SE (h1)

t1/2 (h)

r2

0.053 ± 0.005 a 0.049 ± 0.004 a 0.016 ± 0.003 b

13.2 14.2 42.9

0.98 0.96 0.93

0.055 ± 0.004 a 0.044 ± 0.01 ab 0.031 ± 0.007 b

12.6 16.5 23.3

0.96 0.89 0.94

0.027 ± 0.003 a 0.016 ± 0.001 b 0.010 ± 0.0007 c

26.3 43.5 63.5

0.98 0.97 0.97

Regression curves were produced by using first-order kinetics. k (h-1)，t1/2 (h) and r2 represent degradation rate. Constant, half-life and correlation coefficient, respectively. Values are means ± SD (n ¼ 3). According to the Duncan’s multiple range test, different letters in the same column indicate significant differences between treatments (p < 0.05).

DMDS. Other fumigants such as 1,3-dichloropropene (1,3-D) and methyl bromide degraded more slowly in soil at the higher doses (Ma et al., 2001; Guo and Gao, 2009). Ashworth et al. (2018) also showed that the degradation rate of a fumigant in soil decreased as the dose increased and, importantly, emissions to air increased as the dose increased. In commercial practice, the appropriate application dose of AITC and other fumigants should be determined based on the soil texture to achieve optimal control of pests and weeds.

3.5. Effects of soil moisture on the rate of AITC degradation in soil The AITC degradation data were a good fit (r2 values 0.93e0.99) to first-order kinetics when Suihua soil was dosed with AITC at temperatures of 4e48  C and 3e30% moisture content (Table 4). The half-life values of AITC degradation in soil decreased with increasing water content, even under low temperature conditions. The effect of soil water content on the degradation of fumigants has been well documented (Qin et al., 2009; Fang et al., 2018; Han et al., 2018). An increase in moisture content increases the pore size of the soil, increases the concentration of the fumigant in the aqueous phase and facilitates the distribution of the fumigant through the soil. Pesticides dissolved in water are more accessible

Table 4 Degradation of AITC in Suihua soil exposed to temperatures from 4 to 48  C and containing a soil moisture content from 3 to 30%. Temperature( C)

Moisture content (%)

k±SE (h1)

t1/2(h)

r2

4

3 6 12 18 30 3 6 12 18 30 3 6 12 18 30 3 6 12 18 30 3 6 12 18 30

0.0033 ± 0.0003 0.0058 ± 0.0001 0.0092 ± 0.0002 0.017 ± 0.002 0.019 ± 0.001 0.0035 ± 0.0006 0.0082 ± 0.0006 0.014 ± 0.0007 0.043 ± 0.007 0.077 ± 0.01 0.0049 ± 0.001 0.023 ± 0.0008 0.032 ± 0.002 0.073 ± 0.007 0.076 ± 0.01 0.012 ± 0.001 0.037 ± 0.01 0.071 ± 0.007 0.069 ± 0.003 0.093 ± 0.01 0.019 ± 0.005 0.064 ± 0.03 0.098 ± 0.005 0.16 ± 0.01 0.17 ± 0.005

210.5 119.9 75.6 42.1 36.8 199.0 84.7 49.5 16.0 9.0 140.1 30.2 21.8 9.5 9.1 59.9 18.8 9.7 10.1 7.5 35.6 10.8 7.1 4.4 4.2

0.98

18

28

38

48

0.92

0.93

0.93

0.99

Regression curves were produced by using first-order kinetics. k (h-1)，t1/2 (h) and r2 represent degradation rate constant, half-life and correlation coefficient, respectively. Values are means ± SD (n ¼ 3).

to soil microbes (Ogram et al., 1985; Smelt et al., 1989; Long et al., 2014). Guo (2004) showed that hydrolysis is the main pathway for degrading 1,3-D in soil. Elevated soil water content promotes the hydrolysis reaction, reduces 1,3-D adsorption by soil and increases the dissolution of 1,3-D in water. In our research, an elevated water content (such as 30%) could have promoted the activity of soil microorganisms and accelerated the hydrolysis of AITC. AITC has a solubility coefficient in water of 2 g L1 (at 20  C) (Lashkari, 2017), which is higher than most fumigants. The AITC structure contains two p bonds and exists between nitrogen and sulfur atoms with different electronegativity. Hence, p electrons are easily transferred to atoms with stronger electronegativity, and as a result, carbon atoms are easily reacted with charged reagents, that is, H2O, OH, etc. (Liqin, 1999). Therefore, in soils with higher water content, thiocyanate is easy to combine with water molecules to form intermediates, thus accelerating the degradation rate of AITC. In addition, soil containing water promotes the propagation and growth of soil microorganisms, which are available to accelerate the degradation of fumigants (Han et al., 2018). When soil water is saturated, the activity of aerobic microorganisms is inhibited and the activity of anaerobic microorganisms is increased. Soil moisture may affect the rate of biodegradation directly by inhibiting microbial activity (Shelton and Parkin, 1991). In our research, when the soil water content reached water saturation (at about 30%), the degradation rate of AITC was still faster than at 3, 6, 12, 18% water content at 4e48  C. There may be some anaerobic or facultative anaerobic bacteria alongside AITC-degrading bacteria that decompose AITC even in when the soil water content is elevated. 3.6. Effects of temperature on the AITC degradation rate in soil Soil temperature is one of the key environmental variables that governs the degradation of fumigants. Under five water content conditions, the degradation rates of AITC in Suihua soil generally increased with increasing temperatures (Fig. 1), in accordance with previous studies (Borek et al., 1995). Under dry soil conditions (3% water content), the degradation rate of AITC below 38  C was not significant. This may be due to the inhibition of microbial activity in the arid soil, which affected microbial degradation. Chowdhury et al. (2011) has confirmed this speculation. However, the effect of high temperature on the degradation rate of AITC was significant which demonstrated that the degradation of AITC under dry conditions will be mainly promoted by temperature. When the soil water content is 6%, with the increase of temperature, the degradation rate of AITC gradually accelerated. When the culture temperature was higher than 18  C, the impact of temperature on the degradation was more significant. Relatively high temperatures and available water may promote the survival of AITC degradation bacteria in the soil, and also accelerate the hydrolysis reaction of AITC itself. Besides, the degradation rate response of AITC with 12% water content to temperature was

J. Liu et al. / Chemosphere 244 (2020) 125540

Fig. 1. The degradation rate of AITC in Suihua soil under five temperatures from 4 to 48  C and soil moisture from 3 to 30%. According to the Duncan’s multiple range test, different letters indicate significant differences between treatments (p < 0.05).

consistent with that of 6% water content. The trend of degradation rate of temperature response was roughly the same when the soil water content is 18% and 30%. When the water content was 18%, the degradation rate of 48  C was 2.2e9.4 times that of the other four temperatures. Similarly, the degradation rate at 30% water content is 1.8e8.9 times. Temperature controls the process of most chemical and microbial reactions. In general, the rate of degradation of fumigants increases with increasing soil temperature (Gan et al., 1999; TaylorLovell et al., 2002). Van’t Hoff approximation rule has shown that the reaction velocity will increase by 2e3 times for every 10  C increase in temperature (van’t Hoff, 1896). And Previous research demonstrated that when the temperature was raised by 30  C, the degradation rate of the fumigant was also increased by 7 times (Gan et al., 1999). Microorganisms require certain environmental conditions for optimal growth and utilization of any fumigants. The main factors affecting the abundance and activity of microorganisms are temperature, moisture, pH and nutrients (Gan et al., 2000). In general, warm and fertile soil promotes microbial growth and will therefore enhance the degradation of fumigants. Gan et al. (2000) found that the relationship between microbial degradation and temperature also depended on the fumigant itself. For example, when the temperature was higher than 30  C, microbial degradation of 1,3-D was inhibited and microbial degradation of Methyl isothiocyanate (MITC) was reversed. Similarly, the microbial activity of chloropicrin was not inhibited by high temperatures (Gan et al., 2000), which was consistent with our results for AITC. At temperatures of 38 and 48  C, the degradation of AITC was not inhibited, possibly because temperatures above 38  C have a reduced impact on biological and chemical reaction processes. 4. Conclusions In our experiment, we firstly developed a simple and efficient AITC extraction method that used ethyl acetate as the extraction reagent, vortex for 1 min and hold for 30 min. Then we investigated which factors affected the degradation of AITC in the soil, by collecting samples from nine regions and analyzing the correlation between their respective physical and chemical indicators and the degradation rate. We conclude that available nitrogen and electrical

7

conductivity were major factors influencing the degradation of AITCd degradation rate was significantly positively correlated with conductivity and available nitrogen. Compared with chemical degradation, AITC’s biodegradation accounted for a larger proportion. In addition, the degradation of AITC was affected by the application dose, specifically, as the dose administered increases, the rate of degradation gradually decreases. Correlation analysis showed that there was a significant negative correlation between the degradation rate at different application doses and the proportion of clay in the soil texture. Soil water content is an important environmental factor affecting the degradation of AITC, and the half-life values of AITC degradation decreased with increasing water content, even under low temperature conditions. Another important environmental factor is the culture temperature. The degradation rates of AITC generally increased with increasing temperatures. High temperature and high humidity have an absolute driving effect on the degradation of AITC. The use of AITC in commercial practice will be a compromise between slow degradation to allow sufficient time for AITC to be effective against key pests and diseases, and fast degradation to minimize the impact of AITC on the environment. Our research results may be useful for developing a decision support system to control soil-borne pests and diseases based on AITC, and further guidance for those using AITC in the field. Funding This research was supported by the Key Research and Development Program of China (2017YFD0201600). Notes The authors declare no competing financial interest. Acknowledgments The author is grateful for the financial support from Key Research and Development Program of China (2017YFD0201600). Financial support from the Natural Science Foundation Project of Beijing (6172029). The author also thanks Dr Tom Batchelor for editing the draft manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.chemosphere.2019.125540. Author contributions Jie Liu and Qiuxia Wang designed the study and wrote the protocol; Jie Liu, Xianli Wang and Bin Huang collected the soil samples; Jie Liu, Wensheng Fang and Yi Zhang carried out determination of soil physicochemical properties; Jie Liu, Aocheng Cao, Dongdong Yan, Canbin Ouyang and Yuan Li managed the literature search and analyses; Jie Liu performed most of the experiments; Jie Liu, Qiuxia Wang, Xianli Wang and Dawei Han analyzed the data; Jie Liu and Qiuxia Wang were responsible for the overall design and wrote the manuscript. References Aislabie, J., Lloyd-Jones, G., 1995. A review of bacterial-degradation of pesticides. Soil Res. 33, 925e942, 1838-6768. Ashworth, et al., 2018. Application rate affects the degradation rate and hence emissions of chloropicrin in soil. Science of the Total Environment. Bangarwa, S.K., Norsworthy, J.K., Gbur, E.E., Zhang, J., Habtom, T., 2011. Allyl

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