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1 1 Postharvest Application of Boric Acid on Grape to Improve Shelf 2 life and Maintain the Quality 3 4 Hui Jie Lia,b, Jia Bing Jiaoa,b, Yi Man Fanga,b, Yang Yang Zhanga,b, Da Long Guoa,b 5 a College of Horticulture and Plant Protection, Henan University of Science and Technology, 6 Luoyang 471023, P R China 7 b Henan Engineering Technology Research Center of Quality Regulation and Controlling of 8 Horticultural Plants, Luoyang 471023, P R China 9 Corresponding author Da Long Guo, E mail guod.
1 Postharvest Application of Boric Acid on Grape to Improve Shelf- life and Maintain the Quality Hui-Jie Lia,b, Jia-Bing Jiaoa,b, Yi-Man Fanga,b, Yang-Yang Zhanga,b, Da-Long Guoa,b* a Luoyang 471023, P R China b Horticultural Plants, Luoyang 471023, P R China * Corresponding author: Da-Long Guo, E-mail: guodalong@haust.edu.cn College of Horticulture and Plant Protection, Henan University of Science and Technology, Henan Engineering Technology Research Center of Quality Regulation and Controlling of 10 11 12 13 14 15 16 17 18 19 20 21 22 Electronic copy available at: https://ssrn.com/abstract=4053468 23 ABSTRACT 24 Boric acid (BA) is commercially acceptable and economically feasible material to enhance shelf- 25 life of pear, orange and other horticultural plants Here, we investigated the effect of BA on the 26 shelf-life and postharvest quality of table grape (cv ‘Kyoho’) Grape berries were immersed in BA 27 solution with different concentrations (0.00 [as control], 0.01, 0.03, 0.05 M) for 10 and stored 28 at room temperature for 10 days Compared with the control, BA treatment groups maintained 29 higher berry firmness by inhibiting the activity of polygalacturonase (PG) and cellulase, although 30 not all indexes and treatments had advantages after BA treatment At the same time, BA treated 31 grapes maintained higher antioxidant enzyme activities such as catalase (CAT), superoxide 32 dismutase (SOD) and lower metabolic toxic products like superoxide anion (𝑂2_ ) production rate, 33 malondialdehyde (MDA) and hydrogen peroxide (H2O2) content than control The experiment 34 results showed that postharvest application of BA effectively delay the senescence of grapes 35 compared with the control, and 0.01 M BA treatment had the most obvious effect 36 Keywords: Kyoho, Boric acid, postharvest, antioxidant enzyme 37 38 39 40 41 42 43 44 Electronic copy available at: https://ssrn.com/abstract=4053468 45 1.Introduction 46 Grape (Vitis vinifera L.) is one of the most widely consuming fruits all over the world (Li et al., 47 2018) At present, China has become one of the world's biggest grape producers (Khan et al., 2020) 48 Over 84% of the total land used for grape production in China is cultivated for the table grapes (Sun 49 et al., 2020) However, table grapes, as non-climacteric fruits with thin pericarp and succulent flesh, 50 are easily infected by plant pathogens and exposed to serious water loss, which could result in a 51 high fungal decay rate (Meng et al., 2010) Postharvest senescence and disease have recently 52 seriously restricted the market development of table grapes Therefore, it is necessary to explore 53 some strategies for table grapes storage 54 In this context, different methods such as preharvest and postharvest applications of kombucha 55 (Zhou et al., 2019), short-term high CO2 (Vazquez-Hernandez et al., 2018), Aloe vera gel (Ehtesham 56 Nia et al., 2021), aerosol with calcium-based (Cherviak et al., 2021), edible coatings (1.5% chitosan 57 and 1.0% poly-ε- lysine) (Chen et al., 2019) were used to maintain the firmness and inhibit the decay 58 of fresh table grapes In addition, chemical fungicides are widely used in vineyards to control 59 postharvest diseases of grapes (Ehtesham Nia et al., 2021) However, a large quantity of chemical 60 spraying will lead to adverse effects on consumer health and the environment Hence, more 61 environmentally friendly and economical methods need to be explored urgently to solve these 62 problems preferably 63 Boron was accepted as an essential nutrient for all vascular plants, animals and humans Boron 64 regulated the metabolic activities by interacting with magnesium, calcium and vitamin D, which are 65 all necessary for bone metabolism (Devirian and Volpe, 2003) Boron has disinfectant and 66 bactericidal properties which inhibits the fruit decay after harvest and plays a crucial role in Electronic copy available at: https://ssrn.com/abstract=4053468 67 maintaining the rigidity of fruit cytoderm and phenolic concentration (Kaur et al., 2019) It was 68 reported that boron has a good effect on the prevention and control of gray mold of table grapes 69 caused by B cinerea (Qin et al., 2010) Additionally, many studies have revealed that boric acid has 70 chemical properties inhibiting the initial increase of ethylene production (Ahmadnia et al., 2013) 71 and suppressing the activity of ACC synthase and ACC oxidase (Moon et al., 2020) It has also been 72 reported that boric acid enhances the storage life of tomatoes (Wang and Morris, 1992), retains the 73 storability and quality of pear fruits (Kaur et al., 2019), extends shelf life and quality maintenance 74 of Guava (Singh et al., 2017) and improves postharvest quality of Cut Carnation (Ahmadnia et al., 75 2013), and so on However, little information is available on the effect of boric acid application on 76 the postharvest quality of table grapes during storage 77 Accordingly, the objective of the present study was to evaluate the potential of postharvest 78 treatment of boric acid to extend the shelf life of table grape during ambient temperature storage It 79 was hypothesized that different concentrations of boric acid would enhance the storability and 80 quality of table grape (‘Kyoho’) 81 Materials and methods 82 2.1 Plant material and experimental treatment 83 Grape berries of ‘Kyoho’ collecting from a grape vineyard in Luoyang, Henan province, China 84 were employed in this study Grape berries were sampled based on the uniformity in shape and 85 appearance, absence of visible defects All grape samples were harvested after ripening and 86 analyzed at the Henan University of Science and Technology BA solutions at different 87 concentrations (0.00, 0.01, 0.03, 0.05 M) were prepared with distilled water The sampled grape 88 berries were divided into four sets and immersed in four BA solutions for 10 min, then placed at Electronic copy available at: https://ssrn.com/abstract=4053468 89 room temperature for 10 days Samples were taken every days for a total of times, i.e., sampling 90 at 0, 2, 4, 6, 8, 10 days after the treatment, respectively A portion of each sample used for the 91 evaluation of weight loss, berry firmness, and total soluble solid (TSS) content The remain samples 92 were collected and stored at -40 ℃ for subsequent analysis of the physiological indicators 93 2.2 Determination of the weight loss rate, firmness, TSS content 94 95 96 97 The weight of boric acid treated ‘Kyoho’ berries was measured at storage day and 10 storage day using an analytical balance The weight loss rate was calculated by the following formula: Weight loss (%) = Initial weight ‒ final weight × 100 Initial weight The firmness and TSS content of berries treated with BA were measured using the durometer 98 (FT-327, Wuxi, China) and handheld refractometer (WYT-4, Shanghai, China), respectively 99 2.3 Determination of content of ascorbic acid (AsA) 100 AsA was measured according to some modified method (Ge et al., 2015) Frozen tissue was 101 homogenized with 4.0 mL of prechilled 5% metaphosphoric acid and centrifuged at 12,000 rpm for 102 10 at ℃ The supernatant was used to measure the content of AsA The mixture solution was 103 measured at 525 nm, and expressed as mg AsA/g FW A standard curve with ascorbic acid was used 104 to calculate the content of AsA 105 2.4 Determination of the superoxide anion (𝑂𝟐_ ) production rate and content of H2O2 106 The modified method (Ge et al., 2015; Yang et al., 2013) was employed to measure the 𝑂2_ 107 production rate The absorbance of the extracting solution was recorded at 530 nm A standard curve 108 with sodium nitrite was used to calculate the 𝑂2_ production rate following the reaction equation of 109 𝑂2_ with hydroxylamine The production rate of 𝑂2_ was expressed as nmol/min/g FW 110 H2O2 content of the grape berries was measured spectrophotometrically after reaction with Electronic copy available at: https://ssrn.com/abstract=4053468 111 potassium iodide (Chakrabarty and Datta, 2007) The reaction mixture was measured at 390 nm, 10% 112 TCA solution was used as control The content of H2O2 was calculated using a standard curve with 113 known concentrations of H2O2 114 2.5 Determination of SOD activity and CAT activity 115 Superoxide dismutase (SOD) and Catalase (CAT) were extracted and assayed according to the 116 modified methods (Sun et al., 2011) Frozen grape berry tissue was extracted for with 2.0 mL 117 of 0.05 M sodium phosphate buffer (pH 7.8) containing 0.1% (w/v) polyvinyl pyrrolidone The 118 extract solution was centrifuged for 20 at 12,000 rpm at ℃ The supernatant was collected 119 for the determination of SOD activity and CAT activity 120 SOD activity was determined by measuring its ability to inhibit the photochemical reduction of 121 nitro blue tetrazolium (NBT) A total of 0.5 mL of enzyme solution was added into 3.0 mL of assay 122 reagent consisted of 130 mM methionine, 30 μM EDTA, 750 μM NBT, 20 mM riboflavin in 0.05 123 M sodium phosphate buffer (pH 7.8) The reaction solutions were incubated for 20 under 4000 124 lux illumination The absorbance of sample was spectrophotometrically measured at 560 nm and 125 0.05 M sodium phosphate buffer (pH 7.8) was used as control The SOD activity was expressed as 126 U/g FW, where 1U is the amount of enzyme that caused 50% inhibition of NBT reduction 127 The assay mixture for determining CAT activity consisted of 0.3 mL of 0.1 M H2O2 prepared by 128 0.05 M sodium phosphate buffer (pH 7.8) and 0.5 mL of enzyme solution The decrease in 129 absorbance at 240 nm was recorded for at 25 ℃ And the CAT activity was expressed as U/g 130 FW/min, where 1U was defined as the amount of enzyme that caused a change of 0.01 in absorbance 131 per minute 132 2.6 Determination of malondialdehyde (MDA) content Electronic copy available at: https://ssrn.com/abstract=4053468 133 The modified method (Ehtesham Nia et al., 2021) was employed to measure the MDA content 134 Frozen grape berry tissue was homogenized for in 5.0 mL of 10% (w/v) trichloroacetic acid 135 The homogenate was centrifuged for 15 at 12,000 rpm Three milliliter of the supernatant was 136 added to 3.0 mL of 0.67% (w/v) trichloroacetic acid The mixture solution was heated for 20 at 137 100 ℃, quickly cooled in an ice-bath for 10 and then centrifuged for 15 with12,000 rpm 138 at ℃ Absorbances were measured at 532, 450 and 600 nm MDA concentration was calculated 139 as follows: MDA content (mmol /g FW) = [6.45 (OD532 − OD600) − 0.56OD450] × mL/0.5 g 140 2.7 Determination of polygalacturonase and cellulase activity 141 PG and cellulase activity were measured using described methods (Abu-Sarra and Abu-Goukh, 142 2015) The reaction mixture containing 0.5ml crude enzyme, 2.0 ml 0.5% pectin was incubated at 143 37 ℃ for 30 After the constant temperature reaction, DNS was added, and the mixed solution 144 was boiled for minutes Absorbance was measured at 540nm One pectinase activity unit was 1.0 145 mg galacturonic acid produced by pectin decomposition at 37 ℃ per gram of fresh sample per 146 minute 147 The cellulase activity was determined by the same procedure as PG assay, but the reaction 148 temperature and time was 40 ℃, 60min, and the substrate was 1% carboxymethyl cellulose The 149 cellulase activity unit was 1.0 mg glucose produced by the decomposition of carboxymethyl 150 cellulose at 40 ℃ per gram of fresh sample per minute 151 2.8 Statistical analysis 152 The data presented as mean ± standard deviation (SD) from three replicates were tested using the 153 SPSS 21.0 software Differences at P＜0.05 were considered significant Figures were produced 154 using GraphPad Prism 9.0 Electronic copy available at: https://ssrn.com/abstract=4053468 155 Results 156 3.1 Effects of BA treatment on the weight loss and firmness of ‘Kyoho’ berries 157 In the 0.01 M BA treatment group, the weight loss rate was significantly lower than the control, 158 while there was no significant difference among the other groups (Fig 1A) These data indicate that 159 the three treatments of boric acid are not all beneficial to the index of water loss 160 The firmness of grape berries gradually decreased during storage (Fig 1B), and it was 161 significantly higher in the 0.01 M BA treatment group than that of berries in the other BA treatment 162 and the control groups This suggests that 0.01 M BA treatment could effectively prevent the 163 reduction in grape quality and firmness during storage (Fig 1B) 164 165 Fig Effects of boric acid (BA) treatment on the weight loss rate(A)and firmness(B) of ‘Kyoho’ 166 grape berries The concentrations of boric acid treatment were 0.00, 0.01, 0.03 and 0.05M, 167 respectively Vertical bars indicate mean ± standard deviation (SD) n = replicates The bars 168 followed by the same letter are not significantly different at P＜0.05 169 3.2 Effects of BA treatment on TSS content and AsA content 170 The variation trend of TSS after BA treatment with different concentrations was consistent with 171 that of the control (Fig 2A) Among the BA treatment groups, the 0.03 and 0.05 M BA treatment Electronic copy available at: https://ssrn.com/abstract=4053468 172 group showed the highest TSS contents (Fig 2A) 173 The AsA content of 0.01 M BA treatment grape berries were significantly higher than the control 174 during all storage days (Fig 2B) In addition, the content of AsA in 0.03 M BA treatment was also 175 significantly higher than the control except at the 8th storage day (Fig 2B) 176 177 Fig Effects of boric acid (BA) treatment on the TSS (A)and AsA content (B) of ‘Kyoho’ grape 178 berries The concentrations of boric acid treatment were 0.00, 0.01, 0.03 and 0.05M, respectively 179 Vertical bars indicate mean ± standard deviation (SD) n = replicates The bars followed by the 180 same letter are not significantly different at P＜0.05 181 3.3 Effects of BA treatment on MDA content, superoxide anion (𝑂𝟐_ ) production rate and H2O2 182 content 183 Changes in the MDA content of grapes were shown in Fig 3A The MDA content of berries 184 increased during the first days of storage, reaching the peak on day 4, and then declined from day 185 to day10 At the peak levels, the MDA content was the highest in the 0.03 M BA treatment group 186 and the lowest in the 0.01 M BA treatment group (Fig 3A) During all storage times other than at 187 the 10th storage day, the MDA content in 0.01 M BA treatment was significantly lower than the 188 control These data showed that BA inhibited the production of MDA, and it slowed the senescence Electronic copy available at: https://ssrn.com/abstract=4053468 189 rate of grape berries effectively at a concentration of 0.01 M (Fig 3A) 190 The superoxide anion (𝑂2_ ) production rate of grape berries showed the same increase or decrease 191 trend in all the treatment groups, and the BA treatment groups was lower than the control group on 192 the whole especially in 0.01 M BA treatment group (Fig 3B) Additionally, the 0.01 BA treatment 193 had the lowest hydrogen peroxide content in grape berries among all the treatments (Fig 3C) 194 195 Fig Effects of boric acid (BA) treatment on MDA content (A), superoxide anion (𝑂2_ ) production 196 rate(B) and H2O2 content(C) of ‘Kyoho’ grape berries The concentrations of boric acid treatment 197 were 0.00, 0.01, 0.03 and 0.05M, respectively Vertical bars indicate mean ± standard deviation 198 (SD) n = replicates The bars followed by the same letter are not significantly different at P＜ 199 0.05 200 3.4 Effects of BA treatment on SOD and CAT activities 10 Electronic copy available at: https://ssrn.com/abstract=4053468 201 SOD activity showed similar profiles among the control and BA treatment groups (Fig 4A) The 202 activity of SOD went up and down three times but the overall activity was increasing gradually 203 during storage (Fig 4A) The SOD activity of 0.01M BA group was higher than that of the control 204 group on the whole (Fig 4A) 205 The CAT activity profile was similar among the different BA treatments and the control, with a 206 gradual increase from day to day and from day to day 6, followed by a decrease from day to 207 day and from day6 to day 10 (Fig 4B) The activity of CAT was significantly higher in the 0.01 208 M BA treatment group than in the control from day to day During the storage, the highest CAT 209 activity was detected on day6 in 0.01 M BA treated berries (Fig 4B) 210 211 Fig Effects of boric acid (BA) treatment on SOD(A) and CAT(B) activities in ‘Kyoho’ grape 212 berries The concentrations of boric acid treatment were 0.00, 0.01, 0.03 and 0.05M, respectively 213 Vertical bars indicate mean ± standard deviation (SD) n = replicates The bars followed by the 214 same letter are not significantly different at P＜0.05 215 3.5 Effects of BA treatment on PG and cellulase activities 216 The activities of PG and cellulase in 0.01 M treatment group were lower than that in control group 217 as a whole (Fig 5) The PG activity increased gradually and then stabilized in a certain range (Fig 11 Electronic copy available at: https://ssrn.com/abstract=4053468 218 5A), moreover, the cellulase activity in grape berries increased firstly, then decreased slightly, and 219 significant differences were observed among various BA treatment groups (Fig 5B) 220 221 Fig Effects of boric acid (BA) treatment on PG(A) and cellulase(B) activities in ‘Kyoho’ grape 222 berries The concentrations of boric acid treatment were 0.00, 0.01, 0.03 and 0.05M, respectively 223 Vertical bars indicate mean ± standard deviation (SD) n = replicates The bars followed by the 224 same letter are not significantly different at P＜0.05 225 Discussion 226 It is essential to maintain the postharvest quality of grape during storage days which is mostly 227 consumed in fresh state (Jung et al., 2018) To improve the shelf life of table grapes, delaying the 228 progression of grape decay because of senescence is very important Senescence is a complex 229 genetic programming process that is used to describe a series of events that culminate in cell death 230 at the last of a development period, including structural deterioration and macromolecule 231 degradation (Noodén et al., 1997) In table grape, senescence is closely related to reactive oxygen 232 species (ROS) accumulation (Zhang et al., 2019) The excessive production of ROS damages the 233 cells and accelerates the senescence of grapes Plant cells have developed two main scavenging 234 mechanisms of ROS under oxidative stress which can be categorized as enzymatic system and non- 12 Electronic copy available at: https://ssrn.com/abstract=4053468 235 enzymatic system (Shao et al., 2008) In this study, boric acid treated grapes had lower H2O2 content 236 and superoxide anion (𝑂2_ ) production rate than of the control except for individual storage days in 237 the 0.03 M treatment group (Fig 3), indicating that boric acid treatment may control the excessive 238 production of ROS to a certain extent during storage of table grape Meanwhile, boric acid treated 239 grape maintained significantly slightly higher CAT activity and SOD activity than control and the 240 highest CAT activity was detected on the 6th day of storage in 0.01 M BA treated berries (Fig 4) 241 Membrane deterioration and degradation is an early and essential characteristic of signal 242 transduction pathway that occur in plant senescence (Bhattacharjee, 2005; Fan et al., 1997) In the 243 meantime, as the major cause of plant cell senescence, peroxidation of membrane lipids leads to the 244 loss of membrane integrity, physical structure, and fluidity, which further affects protein function 245 (Shewfelt and Del Rosario, 2000) Loss of membrane integrity is associated with the senescence of 246 grapes, which accompanied by the disorder of ROS, especially the high levels of H2O2 and MDA 247 Malondialdehyde, as a toxic by-product of ROS metabolism and the end product of lipid 248 peroxidation, has been used to reflect the degree of cell membrane lipid peroxidation (Hodges et al., 249 1999) The MDA content of 0.01and 0.05 M BA treatment groups were lower than that of the control, 250 and the MDA content of 0.01 M BA treatment group was the lowest However, compared with the 251 control group, the 0.03 M treatment group had no significant effect on reducing the MDA content 252 (Fig 3A) The measurement results of hydrogen peroxide content (Fig 3C) in the samples were 253 similar to MDA, described as above-mentioned The results showed that BA treatment significantly 254 reduced the over-production of MDA and H2O2 during storage period and inhibited lipid 255 peroxidation This possibly is related to the previous discovery that boron helps maintain plasma 256 membrane integrity by stimulating the activity of ATPase (Ferreira et al., 2021; Ganie et al., 2013) 13 Electronic copy available at: https://ssrn.com/abstract=4053468 257 In the previous study, some reports demonstrated that boron could control disease in grapevine 258 caused by fungus and gray mold on table grapes caused by B cinerea (Estevez-Fregoso et al., 2021; 259 Qin et al., 2010) Additionally, Boric acid is commercially acceptable and economically feasible 260 and environmentally safe management strategy to enhance shelf life of a lot of horticultural plants 261 In the present experiment, there was a reduction in fruit firmness with a storage period in boric acid 262 treated as well as control fruit, and the 0.01 M BA treatment group maintained the highest firmness 263 of grape berries (Fig 1B) This probability due to the function of boron in the synthesis of cell wall 264 composition (Liu et al., 2014; Matoh, 1997) The role of borates as antifungal complex in the control 265 of postharvest diseases in various fruits has also been demonstrated (Shi et al., 2011) In addition, 266 this may be concerned with the revelation that boric acid keeps the cell wall rigid by forming links 267 to the carboxyl groups of pectin compounds in the cell wall (O'Neill et al., 2004) This binding 268 resists cell wall deterioration enzymes, including polygalacturonase, cellulase, and inhibits the rate 269 of softening during storage Meanwhile, BA treated grapes maintained significantly low PG activity 270 and cellulase activity (Fig 5), which often caused fruit softening and degradation of cell wall 271 components due to depolymerization of celluloses, hemicelluloses and pectin substances which 272 decreased the thickness and rigidity following the degradation of cellulose fiber (Chen et al., 2017; 273 Ge et al., 2019) It is presumably because this element improves carbohydrate metabolism and 274 translocation, whose effect is to provide a substrate for cell respiration and cell wall synthesis It is 275 also reported to play a role in processes such as cell capture and transport, cell wall formation, cell 276 membrane function and antioxidant defense system (Riaz et al., 2021) 277 Our results indicated that postharvest application of BA delayed the senescence process of grapes 278 In general, 0.01 M BA treatment had the best fresh-keeping effect First, antioxidant enzymes 14 Electronic copy available at: https://ssrn.com/abstract=4053468 279 maintained high activity The other is the toxic by-product of aerobic metabolism, which is kept 280 low However, the 0.03 and 0.05 M treatment groups did not have significant advantages in all 281 indicators, especially in water loss, which may be caused by high or inappropriate concentration 282 Consequently, senescence of grape berries during storage is moderated by BA treatment 283 Conclusions 284 The present study explored the effect of boric acid on the storage performance of grape berries at 285 room temperature, and further explored the appropriate concentration of BA for postharvest 286 preservation of grape BA alleviated postharvest senescence of grape to some extent and 0.01 M 287 BA 288 was found most effective in improving the quality of grape after harvest by maintaining higher berry 289 firmness, AsA content and moisture content Moreover, it also resulted in lower MDA content, 290 superoxide anion (O2_ ) production rate and H2O2 content during storage Compared with the control, 291 the activities of PG and cellulase enzymes were also lower in 0.01 M BA treated berries Above all, 292 0.01 M BA postharvest treatment is an effective means to prolong the storage life of grape 293 Author contributions 294 Manuscript writing: H.J.L Experiments performance: H.J.L, J.B.J, Y.M.F, Y.Y.Z Manuscript 295 revision and confirmation: D.L.G Data analysis: H.J.L All authors read and approved the final 296 manuscript 297 Declaration of Competing Interest 298 299 300 The authors declare that there is no conflict of interest in this study Acknowledgments This work was financially supported by Natural Science Foundation of China (NSFC: U1904113), 15 Electronic copy available at: https://ssrn.com/abstract=4053468 301 National Key Research and Development Program of China (2018YFD1000105), and Program for 302 Innovative Research Team (in Science and Technology) in University of Henan Province 303 (21IRTSTHN021) 304 305 References 306 Abu-Sarra, A.F., Abu-Goukh, A.A., 2015 Changes in pectinesterase, polygalacturonase and cellulase 307 activity 308 http://10.1080/00221589.1992.11516284 during mango fruit ripening J Hortic Sci 67, 561-568 309 Ahmadnia, S., Hashemabadi, D., Sedaghathoor, S., 2013 Effects of boric acid on postharvest 310 characteristics of cut Carnation (Dianthus caryophyllus L cv.‘Nelson’) Ann Biol Res 4, 242-245 311 Bhattacharjee, S., 2005 Reactive oxygen species and oxidative burst: Roles in stress, senescence and 312 signal transducation in plants Curr Sci 1113-1121 313 Chakrabarty, D., Datta, S.K., 2007 Micropropagation of gerbera: lipid peroxidation and antioxidant 314 enzyme activities during 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