Article Cite This: J. Agric. Food Chem. 2017, 65, 9987-9994
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Natural Variation in Banana Varieties Highlights the Role of Melatonin in Postharvest Ripening and Quality Wei Hu,†,‡ Hai Yang,†,§ Weiwei Tie,‡ Yan Yan,‡ Zehong Ding,‡ Yang Liu,‡ Chunlai Wu,‡ Jiashui Wang,∥ Russel J. Reiter,⊥ Dun-Xian Tan,⊥ Haitao Shi,*,# Biyu Xu,*,‡ and Zhiqiang Jin*,‡,∥ ‡
Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Xueyuan Road 4, Haikou, Hainan 571101, People’s Republic of China § National Engineering Research Center for Nanomedicine, College of Life Science and Technology, Huazhong University of Science and Technology, Luoyu Road 1037, Wuhan, Hubei 430074, People’s Republic of China ∥ Key Laboratory of Genetic Improvement of Bananas, Hainan Province, Haikou Experimental Station, China Academy of Tropical Agricultural Sciences, Haikou, Hainan 570102, People’s Republic of China ⊥ Department of Cellular and Structural Biology, The University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, Texas 78229, United States # Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources and College of Biology, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, Hainan 570228, People’s Republic of China S Supporting Information *
ABSTRACT: This study aimed to investigate the role of melatonin in postharvest ripening and quality in various banana varieties with contrasting ripening periods. During the postharvest life, endogenous melatonin showed similar performance with ethylene in connection to ripening. In comparison to ethylene, melatonin was more correlated with postharvest banana ripening. Exogenous application of melatonin resulted in a delay of postharvest banana ripening. Moreover, this effect is concentrationdependent, with 200 and 500 μM treatments more effective than the 50 μM treatment. Exogenous melatonin also led to elevated endogenous melatonin content, reduced ethylene production through regulation of the expression of MaACO1 and MaACS1, and delayed sharp changes of quality indices. Taken together, this study highlights that melatonin is an indicator for banana fruit ripening in various varieties, and the repression of ethylene biosynthesis and postharvest ripening by melatonin can be used for biological control of postharvest fruit ripening and quality. KEYWORDS: banana, ethylene, melatonin, postharvest ripening, quality
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a profound role in the regulation of fruit ripening and quality.4,8−10 In the last 20 years, many studies focused on ethylene biosynthesis and signaling transduction during the fruit ripening process.4,7,11−13 Besides ethylene, the other crucial regulators potentially underlying fruit ripening have been largely ignored. In the late 1950s, melatonin (N-acetyl-5-methoxytryptamine) was initially found in the pineal gland of cows.15,16 In 1995, melatonin was identified in plants.17,18 Thus far, melatonin has been discovered in various plant species, including Arabidopsis, rice, tobacco, strawberry, apple, cucumber, etc.19 On the basis of physiological, biochemical, and genetic evidence, melatonin plays multiple roles in plants, such as seed germination, vegetative growth, flower development, photoprotection, root architecture, leaf senescence, and response to biotic and abiotic stresses.19−21 However, the roles of melatonin in postharvest ripening and fruit quality regulation are less known. Cultivated bananas originate from either intraspecific hybridizations between wild diploid subspecies of Musa acuminata or interspecific crosses between M. acuminata and the wild diploid
INTRODUCTION Banana, a typical climacteric fruit, undergoes a postharvest ripening process characterized by a green-storage phase, followed by the climacteric period.1−3 There are various physiological and biochemical changes during the climacteric period, such as flavochrome accumulation, chlorophyll breakdown, degradation of the cell wall components resulting in fruit softening, and degradation of the starch into soluble sugar. These changes affect quality of the banana fruit, including fruit color, firmness, aroma, astringency, and shelf life.1 As a result, the postharvest ripening process is of great importance to improve the quality of banana fruit as well as extend the shelf life. Different ripening periods among various varieties exist in banana, and the natural variation provides valuable clues to the agronomical traits. To aid the development of the banana industry, it is essential to identify the crucial regulators and the underlying molecular mechanism of natural variation in postharvest ripening and quality. During the postharvest ripening process, a burst of ethylene production occurs coincident with the fruit climacteric period.4 Ethylene production of climacteric fruits regulates many ripening/quality-related events.1 Moreover, exogenous ethylene greatly accelerates the ripening process, whereas exogenous 1-methylcyclopropene (1-MCP), an ethylene receptor inhibitor, significantly delays the ripening process.5−7 Thus, ethylene plays © 2017 American Chemical Society
Received: Revised: Accepted: Published: 9987
July 24, 2017 October 18, 2017 October 27, 2017 October 27, 2017 DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
Article
Journal of Agricultural and Food Chemistry Musa balbisiana.22 These combinations resulted in various genetic variance of traits, such as the fruit ripening process, fruit quality, and tolerance stresses. Using typically genetic variance materials is necessary to uncover the general and differential mechanisms underlying fruit ripening. In the present study, various banana varieties with contrasting ripening periods were chosen for natural variation analysis. The direct link between melatonin and postharvest ripening/ ethylene was revealed.
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melatonin was measured with a plant melatonin enzyme-linked immunosorbent assay (ELISA) kit (Jianglai Biotechnology, Shanghai, China) based on the protocols of the manufacturer. Quantification of Endogenous Ethylene Production. Banana fruit samples were enclosed into an airtight container for 2 h at 25 °C to collect ethylene. Ethylene production was examined by an ethylene determinator (GT901, Keernuo, Shenzhen, China). The ethylene production was obtained as recommended by the manufacturer. Assays of Fruit Firmness, Starch, and Soluble Sugar. Fruit firmness was measured using a penetrometer (model GY-3, TuoPu Equipment, Hangzhou, China) according to the instructions of the manufacturer. A peel from one side of the banana finger was removed, and measurements were performed at three different spots. The average of three readings was calculated as the measure of firmness for individual fruits. Starch and soluble sugar contents were determined using previously described methods.25 RNA Isolation and Real-Time Reverse Transcription Polymerase Chain Reaction (RT-PCR) Analysis. The banana fruits after various treatments were sampled to extract total RNA. First-strand cDNA was synthesized by SuperScript reverse transcriptase (Takara) in a 20 μL reaction volume, which was subsequently used as the template in real-time RT-PCR. Before quantitative analysis, a series of primer and template dilutions were examined to determine the optimal concentrations. Specificities of primer pairs were determined by agarose gel electrophoresis, melting curve, and sequencing analyses (Supplemental Table S1 of the Supporting Information). Amplification efficiencies for primer pairs were between 0.91 and 1.04. Quantitative experiments were carried out with SYBR Premix Ex Taq (Takara) on a Stratagene Mx3000P (Stratagene, La Jolla, CA, U.S.A.) machine using SYBR chemistry. Expression levels of each target gene were normalized by the internal control MaActin1 and calculated by the 2−ΔΔCT method.26
MATERIALS AND METHODS
Plant Materials and Growth Conditions. Hands of mature unripe bananas were obtained from the banana plantation of the Institute of Tropical Bioscience and Biotechnology (Chengmai, Hainan, China). Fruits from the same hand were harvested and washed with distilled water. Banana hands were separated into individual fingers representing the same developmental stage.23 After various treatments, banana fingers were cultured under a growth chamber (25 °C, 200 μmol m−2 s−1 light intensity; 16 h light/8 h dark cycle, and 70% relative humidity). Chemical Treatments. To investigate the role of melatonin in four varieties, including M. acuminata L. AAA group cv. Nan Tian Huang (NTH), M. acuminata L. AAA group cv. Bao Dao (BD), Musa ABB PisangAwak (FJ), and M. acuminata L. AA group cv. Huang Di (HD), banana fingers were soaked in water (control) or 50 μM melatonin for 2 h. To study the effects of different concentrations of melatonin on postharvest banana ripening, banana fingers [M. acuminata L. AAA group cv. Brazilian (BX)] were soaked in water (control), 50 μM melatonin, 200 μM melatonin, or 500 μM melatonin for 2 h. Each sample contains three replicates from independent experiments. Postharvest Ripening Assay. According to Pua et al.,14 the degree of the postharvest banana ripening process was divided into seven stages, namely, full green (FG, ripening degree 1), trace yellow (TY, ripening degree 2), more green than yellow (MG, ripening degree 3), more yellow than green (MY, ripening degree 4), green tip (GT, ripening degree 5), full yellow (FY, ripening degree 6), and yellow flecked with brown spots (YB, ripening degree 7). The YB stage is the most advanced stage, when bananas have completely ripened during the postharvest ripening progress. Quantification of Endogenous Melatonin. The extraction of melatonin was performed following the acetone−methanol method with 0.1 g of banana fruit powder.24 The endogenous content of
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RESULTS Correlation between Melatonin and Ethylene in Natural Variation of Banana Ripening during Postharvest. To investigate the correlation between melatonin and ethylene during the postharvest period of banana, endogenous melatonin and ethylene were measured in four varieties under the naturally ripened process (Figure 1). For NTH and BD, it took 16 days to reach the YB stage, which is the most advanced stage when
Figure 1. (A) Photos, (B) melatonin content, and (C) ethylene production of four banana varieties (NTH, M. acuminata L. AAA group cv. Nan Tian Huang; BD, M. acuminata L. AAA group cv. Bao Dao; FJ, Musa ABB PisangAwak; and HD, M. acuminata L. AA group cv. Huang Di) during the postharvest period under normal conditions. Data are means ± standard deviation (SD) calculated from three independent experiments. Each independent experiment had three banana fingers. 9988
DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
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Journal of Agricultural and Food Chemistry
normal conditions, whereas it took 14 days to reach the FY stage after melatonin treatment. When the two varieties were stored for 16 days, naturally ripened banana reached the YB stage, whereas the melatonin-treated banana remained at the FY stage. For FJ and HD, more brown spots were observed in naturally ripened banana compared to that in melatonin-treated banana during 6−8 DPH. These results suggest that exogenous application of melatonin results in a delay of postharvest banana ripening (Figure 3). Further physiological studies showed that the endogenous melatonin content was higher during 6−16 DPH in NTH, 8−16 DPH in BD, 6−8 DPH in FJ, and 2−8 DPH in HD after exogenous melatonin treatment than that under normal conditions (panels A−D of Figure 4). In contrast, the ethylene climacteric peak was delayed for NTH and BD, and ethylene production was lower at 6 DPH for FJ and HD after melatonin treatment compared to naturally ripened banana (panels E−H of Figure 4). This result indicates that exogenous application of melatonin increased the endogenous melatonin content, whereas it delayed the ethylene climacteric peak or repressed ethylene production during postharvest banana ripening. To study the effect of melatonin on fruit quality, fruit firmness, starch, and soluble sugar were measured in the four varieties. In NTH, sharp changes in fruit firmness and levels of starch and soluble sugar developed from 6, 8, and 8 DPH, respectively, under normal conditions, whereas from 10, 10, and 12 DPH, respectively, after melatonin treatment (panels I, M, and Q of Figure 4, respectively). In BD, sharp changes in fruit firmness and
bananas have completely ripened during the postharvest ripening process. For FJ and HD, it only took 8 days to reach the YB stage (Figure 1A). This indicated that NTH and BD ripened significantly faster than FJ and HD. The endogenous melatonin content increased at 2 days postharvest (DPH) in the four varieties, peaked at 12 DPH in NTH and BD, and at 6 DPH in FJ and HD, and then decreased. Similar change trends were also observed for the contents of ethylene production during postharvest life (panels B and C of Figure 1). These results indicated the possible link between melatonin and ethylene in both long- and short-storage varieties. Further analyses suggested that there is a positive correlation between melatonin and ethylene (R2 = 0.54, 0.86, 0.92, and 0.52 in NTH, BD, FJ, and HD, respectively) (panels A−D of Figure 2), between melatonin and ripening (R2 = 0.91, 0.66, 0.76, and 0.91 in NTH, BD, FJ, and HD, respectively) (panels E−H of Figure 2), and between ethylene and ripening (R2 = 0.46, 0.41, 0.65, and 0.44 in NTH, BD, FJ, and HD, respectively) (panels I−L of Figure 2). These results indicate a link between melatonin and postharvest ripening/ethylene. In comparison to the correlation between ethylene and ripening, melatonin was more correlated with postharvest banana ripening. Role of Melatonin in Postharvest Banana Ripening and Quality in Different Varieties. To reveal the role of melatonin in postharvest banana ripening, exogenous melatonin was applied to four banana varieties and then the effect of melatonin on the postharvest process and physiological changes were examined. For NTH and BD, it took 12 days to reach the FY stage under
Figure 2. Correlation (A−D) between melatonin and ethylene, (E−H) between melatonin and ripening, and (I−L) between ethylene and ripening in four varieties of NTH (A, E, and I), BD (B, F, and J), FJ (C, G, and K), and HD (D, H, and L). 9989
DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
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In naturally ripened banana, endogenous ethylene increased from 9 DPH and peaked at 15 DPH. Sharp changes for firmness, starch, and sugar developed at 9 DPH. However, endogenous ethylene increased from 12, 15, and 15 DPH and peaked at 17, 19, and 19 DPH after 50, 200, and 500 μM melatonin treatment, respectively. Accordingly, sharp changes for firmness, starch, and sugar developed at 12 DPH after melatonin treatments (panels A−D of Figure 6). These results document that different concentrations (50−500 μM) of melatonin significantly delay the climacteric periods of ethylene and quality. Musa 1-aminocyclopropane-1-carboxylate oxidase 1 (MaACO1) and Musa 1-aminocyclopropane-1-carboxylate synthase (MaACS1) genes are crucial genes responsible for ethylene biosynthesis in the banana postharvest ripening process.4 Expression analyses indicated that MaACO1 and MaACS1 expression increased at 9 DPH and peaked at 15 DPH in naturally ripened banana, whereas they increased at 12 DPH and peaked at 17 DPH in 50 μM melatonin-treated banana (panels E and F of Figure 6). This is highly correlated with endogenous ethylene production during the postharvest period. Besides, exogenous melatonin could represses MaACO1 expression levels and delay the peak time of MaACO1 and MaACS1 expression during the postharvest period.
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DISCUSSION Banana is a popular fruit and is also a staple food for the largely impoverished continent of Africa.27 Despite the economic and social importance of banana, studies of the banana have proceeded slowly because of the limitation of banana cultivation zones.27 As a result of the nature of typical climacteric fruit, the postharvest ripening process is of great importance to affect quality and shelf life of banana. Previously, ethylene has been demonstrated to have a profound effect on banana postharvest ripening.8−10,13 Although ethylene is an important indicator for climacteric fruit ripening, ethylene is not completely correlated with ripening as a result of the sharp climacteric peak of ethylene during fruit ripening.1,4,8−10 Therefore, it is essential to study the mechanism underlying banana postharvest ripening and identify other regulators besides ethylene during the postharvest period. By comparison of the changes of endogenous melatonin and ethylene during the postharvest period in four banana varieties contrasting in ripening period, the direct link between melatonin and postharvest ripening/ethylene was revealed (Figure 1). Melatonin was more correlated with banana ripening in comparison to ethylene (Figure 2). This is due to the inconsistent change trends between ethylene and ripening before the ethylene climacteric stages. At these stages, although the ethylene increases gradually, the extent is very limited. In contrast, the ripening degrees are significantly developed. In comparison to the change trends between ethylene and ripening, melatonin shows a more consistent change trend with ripening (Figure 1). Thus, melatonin can also be used as an indicator for climacteric fruit ripening. The phenotypic and physiological analyses further confirmed the effect of melatonin on natural variation of banana ripening. Melatonin has a significant effect in delaying ripening in both long- and short-storage varieties (Figure 3), and the effect is dose-dependent (Figure 5). During the ripening process, a series of physiological and biochemical changes occur, including degradation of the cell wall components, resulting in fruit softening and degradation of the starch into soluble sugar.1,14,28−31 The effect of melatonin on quality changes, including firmness, starch, and sugar, further support its role in fruit ripening (Figure 4).
Figure 3. Effect of melatonin on the postharvest ripening process of four varieties. Banana fingers were soaked in water (control) or 50 μM melatonin for 2 h. Then, the banana samples were subsequently kept at 25 °C and allowed to ripen. After incubation for 0, 2, 4, 6, 8, 10, 12, 14, and 16 days, photos were taken. Each sample represented three replicates, and each replicate had three banana fingers.
levels of starch and soluble sugar developed from 8 DPH under normal conditions, whereas from 10, 12, and 8 DPH after melatonin treatment (panels J, N, and R of Figure 4, respectively). In FJ and HD, although the sharp changes in fruit firmness and levels of starch and soluble sugar developed at the same time between melatonin and control, the fruit firmness and starch content were higher and the soluble sugar content was lower after melatonin treatment than that under normal conditions during several stages of fruit ripening (panels K, O, S, L, P, and T of Figure 4, respectively). These results show that exogenous application of melatonin participates in the regulation of postharvest banana quality. Effect of Different Concentrations of Melatonin on Postharvest Banana Ripening and Quality. To further confirm the effect of melatonin on postharvest banana ripening and quality, different concentrations of melatonin were used to treat banana fingers of BX and the postharvest ripening process and physiological indicators were examined. It took 15 days to reach the FY stage in naturally ripened banana, whereas it took 17, 19, and 19 days to reach the FY stage in 50, 200, and 500 μM melatonin-treated banana, respectively (Figure 5). These results show that different concentrations (50−500 μM) of melatonin significantly delay postharvest banana ripening. Moreover, the high concentrations of exogenous melatonin had a more significant effect on the delay of postharvest banana ripening than the low concentrations of exogenous melatonin. 9990
DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
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Journal of Agricultural and Food Chemistry
Figure 4. Endogenous contents of (A−D) melatonin and (E−H) ethylene and changes in (I−L) fruit firmness, (M−P) starch, and (Q−T) soluble sugar during the postharvest banana ripening process under normal or melatonin treatment in four varieties of NTH (A, E, I, M, and Q), BD (B, F, J, N, and R), FJ (C, G, K, O, and S), and HD (D, H, L, P, and T). All of the physiological indices were measured with fresh samples and calculated by fresh weight. Data are means ± SD calculated from three independent experiments. Each independent experiment had three banana fingers.
(panels E and F of Figure 6). Thus, melatonin may delay fruit ripening through repressing ethylene biosynthesis. During banana fruit ripening, although melatonin displayed similar change trends to ethylene, they showed the opposite effect on banana fruit ripening (Figures 1 and 3). As is known, both activation and repression are important cellular behaviors to achieve a biological process. Although ethylene is a crucial regulator in inducing fruit ripening, it is possible that ethylene levels need to maintain a balance during the fruit ripening process. As a result of the inhibition effect of melatonin in banana ripening and ethylene production (Figures 3 and 6), melatonin
Ethylene has a profound effect on inducing climacteric fruit ripening.8−10,13 In this study, we found that melatonin had an effect on repressing ethylene biosynthesis. First, exogenous application of melatonin increased the endogenous melatonin content, whereas it repressed ethylene production during postharvest banana ripening in four varieties (Figure 4). Second, different concentrations of melatonin treatments led to repression of ethylene production during the postharvest process (Figure 6A). Lastly, MaACO1 and MaACS1, two crucial genes responsible for ethylene biosynthesis,4 were inhibited by melatonin treatment in the postharvest banana ripening process 9991
DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
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Journal of Agricultural and Food Chemistry
Figure 5. Effect of different concentrations of melatonin on the postharvest ripening process of BX. Banana fingers were soaked in water (control), 50 μM melatonin, 200 μM melatonin, and 500 μM melatonin for 2 h. Then, the banana samples were subsequently kept at 25 °C and allowed to ripen. After incubation for 0, 3, 6, 9, 12, 15, 17, and 19 days, photos were taken. Each sample represented three replicates, and each replicate had three banana fingers.
Figure 6. Changes in (A) ethylene, (B) fruit firmness, (C) starch, (D) soluble sugar, and expression of (E) MaACO1 and (F) MaACS1 during the postharvest banana ripening process under normal or melatonin treatment in BX. The mRNA fold difference was relative to that of control samples at 0 DPH used as a calibrator. All of the physiological indices were measured with fresh samples and calculated by fresh weight. Data are means ± SD calculated from three independent experiments. Each independent experiment had three banana fingers.
possibly acts as an inhibition factor of ethylene. Thus, high levels of ethylene need high levels of melatonin to balance. Finally, melatonin showed a similar change trend with ethylene during the banana ripening process (Figure 1).
Melatonin was reported to accumulate in mature tomato fruits and seeds, and the melatonin content showed increases from the mature green stage to the red stage in the pericarp of tomato fruit.32,33 Recently, melatonin was demonstrated to induce 9992
DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
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Journal of Agricultural and Food Chemistry postharvest ripening and improve the quality of tomato.34,35 It seems that melatonin has opposite effects on the regulation of fruit ripening in banana and tomato. The reasons can be summarized as follows. First, the proper postharvest ripening temperature is 25−28 °C for banana, whereas it is 13−15 °C for tomato.1,4,35 Much evidence confirmed that melatonin responds to different temperatures.19,36−39 It is possible that the different storage temperatures may affect the role of melatonin in postharvest fruit ripening. Second, the behavior of melatonin on ethylene is complicated. In the banana postharvest ripening process, exogenous melatonin represses ethylene biosynthesis through depressing 1-aminocyclopropane-1-carboxylate oxidase (ACO) expression levels and delaying the peak time of 1-aminocyclopropane-1-carboxylic acid synthase (ACS) expression (panels E and F of Figure 6). However, in the tomato postharvest ripening process, exogenous melatonin induces ethylene biosynthesis only by inducing the expression levels of ACS.35 Moreover, melatonin treatment inhibited ethylene production in banana leaves, while combined treatments of melatonin and Fusarium oxysporum f. sp. cubense caused induction of ethylene levels.40 In addition, exogenous melatonin on ethylene signaling transduction is also different in different plant species. The ethylene response factor (ERF)-mediated ethylene pathway was downregulated by melatonin treatment in Arabidopsis,41 whereas it was upregulated by melatonin in bermudagrass.21 On the basis of the above results, the possible molecular mechanism of melatonin and ethylene in regulating postharvest banana ripening is proposed in this study. Melatonin represses the expression of MaACO1 and MaACS1, thus resulting in repression of ethylene biosynthesis and delay of fruit ripening and quality sharp changes. In conclusion, this is the first report revealing the role of melatonin in the regulation of natural variation of postharvest ripening and quality in banana. First, endogenous melatonin shows similar change trends with ethylene during the postharvest period in four banana varieties. Second, melatonin is more correlated with banana ripening in comparison to ethylene, suggesting that melatonin can be used as an indicator for climacteric fruit ripening. Lastly, melatonin-mediated repression of ethylene biosynthesis plays a crucial role in delay of postharvest fruit ripening and sharp changes of quality indices, which could be further used to extend the shelf life of fruits.
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Funding
This work was supported by the earmarked fund for the Modern Agro-Industry Technology Research System (CARS-31), the Central Public-Interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (1630052016005), and the Central Public-Interest Scientific Institution Basal Research Fund for Innovative Research Team Program of Chinese Academy of Tropical Agricultural Sciences (CATAS, 17CXTD-28 and 1630052017017). Notes
The authors declare no competing financial interest.
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ABBREVIATIONS USED 1-MCP, 1-methylcyclopropene; DPH, days postharvest; FY, full yellow stage; YB, yellow flecked with brown spots stage; NTH, Musa acuminata L. AAA group cv. Nan Tian Huang; BD, Musa acuminata L. AAA group cv. Bao Dao; FJ, Musa ABB PisangAwak; HD, Musa acuminata L. AA group cv. Huang Di; BX, Musa acuminata L. AAA group cv. Brazilian; MaACO1, Musa 1-aminocyclopropane-1-carboxylate oxidase 1; MaACS1, Musa 1-aminocyclopropane-1-carboxylate synthase
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.7b03354.
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REFERENCES
Primers used for real-time RT-PCR analysis (Supplemental Table S1) (PDF)
AUTHOR INFORMATION
Corresponding Authors
*Fax: 0086-0898-66160721. E-mail:
[email protected]. *Fax: 0086-0898-66960172. E-mail:
[email protected]. *Fax: 0086-0898-66960172. E-mail:
[email protected]. ORCID
Haitao Shi: 0000-0002-8871-8871 Author Contributions †
Wei Hu and Hai Yang contributed equally to this work. 9993
DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
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DOI: 10.1021/acs.jafc.7b03354 J. Agric. Food Chem. 2017, 65, 9987−9994
