Salicylic-Acid-Induced Chilling- and Oxidative-Stress Tolerance in

Subscriber access provided by CORNELL UNIVERSITY LIBRARY

Article

Salicylic acid-induced chilling- and oxidative-stress tolerance in relation to gibberellin homeostasis, CBF pathway, and antioxidant enzyme systems in cold-stored tomato fruit Yang Ding, Jinhong Zhao, Ying Nie, Bei Fan, Shujuan Wu, Yu Zhang, Jiping Sheng, Lin Shen, Ruirui Zhao, and Xuanming Tang J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.6b02902 • Publication Date (Web): 18 Oct 2016 Downloaded from http://pubs.acs.org on October 19, 2016

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

Journal of Agricultural and Food Chemistry is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 33

Journal of Agricultural and Food Chemistry

1

Salicylic acid-induced chilling- and oxidative-stress tolerance in

2

relation to gibberellin homeostasis, CBF pathway, and antioxidant

3

enzyme systems in cold-stored tomato fruit

4

Yang Ding,† Jinhong Zhao,† Ying Nie,† Bei Fan,† Shujuan Wu,† Yu Zhang,† Jiping

5

Sheng,‡ Lin Shen,§ Ruirui Zhao,§ and Xuanming Tang*,†

6

† Institute of Food Science and Technology, Chinese Academy of Agricultural

7

Sciences, Key Laboratory of Agro-Products Processing, Ministry of Agriculture,

8

Beijing, 100193, China

9

‡ School of Agricultural Economics and Rural Development, Renmin University of

10

China, Beijing, 100872, China

11

§ College of Food Science and Nutritional Engineering, China Agricultural University,

12

Beijing, 100083, China

13

* Corresponding Author

14

Phone: +86-10-62811868;

15

E-mail: [email protected]

16

ACS Paragon Plus Environment


17

Abstract

18

Effects of salicylic acid (SA) on gibberellin (GA) homeostasis, cold-responsive

19

transcription factor (CBF) pathway, and antioxidant enzyme systems linked to

20

chilling- and oxidative-stress tolerance in tomato fruit was investigated. Mature green

21

tomatoes (Solanum lycopersicum L. cv. Moneymaker) were treated with 0, 0.5, and 1

22

mM SA solution for 15 min before storage at 4°C for 28 days. Compared with 0 or 0.5

23

mM SA, 1 mM SA significantly decreased the chilling injury (CI) index in tomato

24

fruit. In the SA-treated fruit, the upregulation of GA biosynthetic gene (GA3ox1)

25

expression was followed by gibberellic acid (GA3) surge and DELLA protein

26

degradation. CBF1 participated in the SA-modulated tolerance and stimulated the

27

expression of GA catabolic gene (GA2ox1). Furthermore, 1 mM SA enhanced

28

activities of antioxidant enzymes, thus reduced reactive oxygen species accumulation.

29

Our findings suggest that SA might protect tomato fruit from CI and oxidative damage

30

through regulating GA metabolism, CBF1 gene expression, and antioxidant enzyme

31

activities.

32

Keywords: tomato fruit; chilling tolerance; salicylic acid; gibberellin homeostasis;

33

CBF pathway; antioxidant enzyme systems

34


Page 2 of 33

Page 3 of 33


35

INTRODUCTION

36

Chilling injury (CI) is a physiological disorder that greatly reduces the

37

postharvest quality of tropical and subtropical fruit and vegetables at low but not

38

freezing temperatures.1 Tomato (Solanum lycopersicum L.) is a typical cold-sensitive

39

fruit that has been used as a model to investigate CI-related metabolism.2 CI

40

macroscopic symptoms of tomato fruit including pitting, browning, and decay usually

41

appear when the fruit are transferred to 20°C to 22°C after storage at 2°C to 6°C for

42

more than 2 weeks.1,3 The development of CI restricts refrigerated transportation and

43

long-term cold storage of harvested tomato fruit, and reduces consumer acceptability

44

leading to substantial economic loss.

45

Salicylic acid (SA) is a natural phenolic compound and endogenous signal

46

involved in the regulation of plant growth, development, and responses to biotic and

47

abiotic stresses.4 Recently, SA exhibits high potential in controlling postharvest losses

48

of horticultural crops such as tomatoes,5 cucumbers,6 and table grapes.4 A few studies

49

have reported that the exogenous application of SA was able to alleviate postharvest

50

CI in tomato fruit.7-10 Mitigation of CI in tomato by SA could be attributed to: (1)

51

inhibition of activities of a variety of membranous lipolytic enzymes, such as

52

phospholipase D and lipoxygenase;7 (2) enhancement of arginine pathway, which

53

leads to the accumulation of signaling molecules, such as polyamines, nitric oxide,

54

and proline;8 (3) stimulation of the synthesis of some stress proteins, such as heat

55

shock proteins,9 pathogenesis-related proteins, and alternative oxidase associated with

56

the avoidance of reactive oxygen species (ROS).10 As chilling stress increases ROS



Page 4 of 33

57

accumulation, the ability to scavenge ROS during and after chilling determines the

58

resistance and adaptation of plants to low temperatures.2 The coordinated action of

59

antioxidant enzymes such as superoxide dismutase (SOD) and catalase (CAT), which

60

are important for scavenging ROS, helps reduce oxidative damage and CI.11 It has

61

been shown that postharvest SA treatment increased the activities of SOD and CAT in

62

cold-sensitive fruit such as mangoes,12 peaches,13 and cucumbers6 at low temperatures.

63

However, the functional relationships among SA, ROS, and related signaling

64

pathways in the responses of postharvest tomato fruit to chilling stress are still poorly

65

understood.

66

Gibberellins (GAs) are important, naturally occurring phytohormones regulating

67

diverse plant growth and development processes throughout the life cycle of higher

68

plants.14 It has been reported that GAs play essential roles in plant responses to

69

various abiotic stress conditions such as salt, oxidative, and heat stresses.15 Recent

70

studies have revealed that exogenous GA3 treatment could effectively alleviate CI

71

symptoms

72

C-repeat/dehydration-responsive element binding factors (CBF) pathway has a vital

73

role in plant responses to cold stress.17 Exogenous GA3 remarkably elevated the

74

expression of CBF1 gene transcripts. Interestingly, GA3 treatment was able to

75

stimulate SA biosynthesis via isochorismate synthase (ICS) pathway in chilled tomato

76

fruit.18 On the other hand, Lee and Park19 pointed out that the transcript levels of GA

77

biosynthetic gene GA3ox1 were elevated by exogenous SA treatment in Arabidopsis

78

seed germination under high-salinity conditions. Emerging evidence suggests the

in

postharvest

tomato

fruit

during


cold

storage.16

Page 5 of 33


79

existence of a cross talk between SA and GA in plants under abiotic stresses. However,

80

tomato is different from Arabidopsis, in that it is susceptible to CI. Little information

81

is available concerning the complex mechanism of hormonal interactions in

82

postharvest fruit during long-term cold storage. Knowing how SA is linked with GA

83

signaling and how antioxidant capacity is regulated by SA would enhance the

84

understanding of the molecular mechanisms underlying SA-GA signaling cross talk in

85

postharvest fruit under chilling and oxidative stresses.

86

The present study aimed to provide a molecular basis to explain the roles of GA

87

homeostasis, CBF1 gene and antioxidant enzyme systems in SA-induced chilling- and

88

oxidative-stress tolerance in tomato fruit. It would provide a more comprehensive

89

insight into the mechanisms underlying SA-GA signaling cross talk in the

90

CBF-mediated stress-response pathway of tomato fruit during long-term cold storage.

91

MATERIALS AND METHODS

92

Fruit Materials and Treatments. Tomato (Solanum lycopersicum L. cv.

93

Moneymaker) fruit were harvested at the mature green stage in October 2014 in a

94

greenhouse under 16 h/8 h (light/dark) photoperiod at 24 °C/19 °C (day/night) in

95

Beijing, China, and transported to the laboratory immediately and stored at 4 °C and

96

80%–90% relative humidity (RH) for 24 h. The mature green stage was determined

97

based on epidermis color (a* = –13 to –10).1 The fruit of uniform size and free from

98

visual blemishes and disease were selected and randomly divided into three lots. The

99

fruit were disinfected with 1% sodium hypochlorite (v/v) for 2 min, washed, and

100

air-dried. Two lots were dipped in aqueous solutions of either 0.5 or 1 mM SA



101

solution [prepared in ethanol/distilled water (1:1000, v/v) containing 0.1% (v/v)

102

Tween-20] for 15 min at 20 °C, respectively. A third lot was dipped in

103

ethanol/distilled water (1:1000, v/v) with 0.1% (v/v) Tween-20 under the same

104

conditions and used as the control. The fruit were stored at 4 °C and 80%-90% RH for

105

28 days. Three replicates of twenty fruit each for control, 0.5 mM SA or 1 mM SA

106

treatment were taken on day 14, 21, and 28 of cold storage for 3 days at 20 °C for CI

107

evaluation. Three replicates of five fruit each for control or 1 mM SA treatment were

108

picked before treatment (time 0) and on day 3, 7, 14, 21 and 28 of cold storage for

109

estimating GA3 content, gene expression, ROS production, and antioxidant enzyme

110

activities. The mesocarp from the fruit equator area was cut into small pieces, frozen

111

in liquid nitrogen, ground to a fine powder and stored at –80 °C.

112

Chilling Injury (CI) Index. The CI index of the chilled fruit was assessed at

113

20 °C for 3 days after 14, 21, and 28 days of cold storage for the development of CI

114

symptoms. Symptoms included surface pitting according to the method of Zhao et al.

115

20

116

pitting; 1, pitting covering less than 25% of the fruit surface; 2, pitting covering

117

25%-50% of the surface; 3, pitting covering 50%-75% of the surface; 4, pitting

118

covering more than 75% of the surface. The average extent of CI was expressed as a

119

CI index, which was calculated as following: CI index (%) = ∑ [(CI level) × (Number

120

of fruit at the CI level)]/[4 × (Total number of fruit)] × 100.

The severity of the symptoms was assessed visually in a four-stage scale: 0, no

121

Gibberellic Acid (GA3) Content. The GA3 content was measured by liquid

122

chromatography-tandem mass spectrometry (LC-MS/MS) following the method of


Page 6 of 33

Page 7 of 33


123

Shi et al. 21 and Zhu et al.18 Frozen tissue (10 g) was weighed into a 50-mL centrifuge

124

tube and extracted using 10 mL of 0.1% (v/v) acetic acid in acetonitrile for 2 min with

125

a vortex mixer. Anhydrous magnesium sulfate (4 g) was added into the tube, and the

126

mixture was centrifuged at 12,000g for 5 min at 4 °C. The extract (1 mL) was filtered

127

with a 0.22-µm membrane, and then analyzed by LC-MS/MS. The chromatographic

128

separation was performed on a Waters XBridge C18 reversed-phase column (2.1 mm

129

× 150 mm, with a 5.0-µm particle size). The gradient condition was shown in Table 1,

130

and the injection volume was 5 µL. The column temperature was maintained at 30 °C

131

with a flow rate of 5 µL s–1. The API5500 tandem quadrupole mass spectrometer

132

(Applied Biosystems, CA, USA) was used for LC-MS/MS analysis and operated in

133

the multiple-reaction monitoring mode. The data was acquired and processed using

134

the AB Sciex Analyst 1.4.2 software (Applied Bioscience, CA, USA). The GA3

135

content was expressed as mg kg–1 fresh weight (FW).

136

RNA Isolation and Reverse Transcription. Total RNA in 2 g of frozen tissue

137

was extracted using an RNAprep Pure Plant Kit (Tiangen, Beijing, China). Total RNA

138

was dissolved in 40 µL of RNase free water, quantified by using a SMA 4000 UV-Vis

139

Spectrophotometer (Merinton, Beijing, China) and stored at -80 °C. Reverse

140

transcription was completed to synthesize the firststrand of cDNA with 1 µg of total

141

RNA according to the instructions from QuantScript RT Kit (Tiangen).

142

Quantitative Real-Time Polymerase Chain Reaction (qPCR). The gene

143

expression changes of GA3ox1 (AB010991), GAI (AY269087), CBF1(AY034473),

144

and GA2ox1 (EF441351) in tomato fruit were studied by quantitative real-time



145

polymerase chain reaction (qPCR) using SuperReal PreMix Plus (SYBR Green)

146

(Tiangen) according to the method of Zhu et al.18 β-actin (SGN-U144149) was used

147

as the reference gene. Specific primers selected from Nation Center for Biotechnology

148

Information (NCBI) were designed from their nucleotide sequences and synthesized

149

by Sangon Biotech Co., Ltd., Company (Shanghai, China) (Table 2). The qPCR

150

amplifications were carried out using an ABI 7500 real-time PCR system (Applied

151

Biosystems). The relative gene expression of the target gene was calculated using the

152

2-∆∆Ct method.22

153

Superoxide Anion (O2•−) Production Rate. The rate of O2•− production was

154

measured by monitoring the formation of nitrite from hydroxylamine as described by

155

Jiang et al.23 with some modifications. Frozen tissue (1 g) was homogenized in an ice

156

bath with 6 mL of 65 mM potassium phosphate buffer (pH 7.8), 2 mL of 10 mM

157

hydroxylamine hydrochloride and 2 mL of 0.1 M ethylenediaminetetraacetic acid

158

(EDTA), and then centrifuged at 12000g for 30 min at 4 °C. The obtained supernatant

159

(2 mL) was mixed with 2 mL of 17 mM 4-aminobenzenesulfonic acid and 2 mL of 7

160

mM α-naphthylamine, and then incubated for 15 min at 40 °C. Ethyl ether (2 mL) was

161

added, and the resulting mixture was centrifuged at 3000g for 15 min. The optical

162

density was recorded immediately at 530 nm. A standard curve for potassium nitrite

163

was used to estimate the production rate of O2•−. The O2•− production rate was

164

expressed as µmol min–1 g–1 FW.

165

Hydrogen Peroxide (H2O2) Content. The assay of H2O2 content was carried out

166

by the procedure previously described by Patterson et al.24 Frozen tissue (1 g) was


Page 8 of 33

Page 9 of 33


167

homogenized in an ice bath with 2 mL of cold acetone and centrifuged at 12,000g for

168

30 min at 4 °C. The supernatant (1 mL) was mixed with 0.1 mL of 5% (w/v) titanium

169

sulfate and 0.2 mL of 17 M ammonia, and then centrifuged at 12,000g for 15 min at

170

4 °C. The precipitate was dissolved in 5 mL of 2 M H2SO4, and then centrifuged for 5

171

min at 12,000g and at 4 °C. The absorbance of the supernatant was measured at 410

172

nm, and H2O2 was quantified using a standard curve generated from known

173

concentrations of H2O2. The H2O2 content was expressed as mmol g–1 FW.

174

Enzyme Assessment. Enzyme extracts for enzyme activity assays were prepared

175

as described previously,2,18 and activities of SOD and CAT expressed as unit U mg–1

176

protein were spectrophotometrically measured using an SOD Detection Kit (A001,

177

Jiancheng, Nanjing, China) and CAT (A007, Jiancheng, Nanjing, China) according to

178

the manufacturer’s instructions.

179

Statistical Analysis. Experiments were performed in triplicate according to a

180

completely randomized design. One-way analysis of variance (ANOVA) and

181

Duncan's multiple range tests were used for statistical evaluations using SPSS

182

(version 19.0) statistical analysis software (IBM SPSS, Inc., IL, USA) with

183

differences being considered significant at P < 0.05. Pearson correlation analysis was

184

used to assess the relationships between GA3 content, gene expressions and enzyme

185

activities.

186

RESULTS AND DISCUSSION

187

Effect of SA on CI index in tomato fruit during storage at 4 °C. CI symptoms

188

in all the fruit appeared after 14 days of 4 °C storage plus 3 days at 20 °C, and



189

continued to progress over time (Figure 1). Compared with the control, 0.5 mM SA

190

treatment significantly inhibited the CI development of fruit, with an index 26% less

191

than that in the control on day 28 (P < 0.05). One millimolar SA remarkably retarded

192

the increase in the CI index, which was 44% less than that in the control at the end of

193

cold storage (P < 0.05). As noted in this figure, treatment with 1mM SA led to the

194

lower CI index compared with the control or 0.5 mM SA. Based on these results, 1

195

mM SA was chosen for further analyses.

196

Effect of SA on GA3 content and GA3ox1 gene expression in tomato fruit

197

during storage at 4 °C. SA has great agronomic potential to improve the stress

198

tolerance of agriculturally important crops.25 However, little information is available

199

on the role of bioactive GA and its signaling components in SA-induced cold

200

tolerance of postharvest fruit during long-term storage. The present study investigated

201

the levels of bioactive GA (GA3) and the expression patterns of a GA biosynthetic

202

gene (GA3ox1) in the control and the SA-treated fruit. The levels of endogenous GA3

203

in the control fruit reduced gradually from day 3 through day 14, and then increased

204

afterward (P < 0.05; Figure 2A). SA treatment notably elevated the GA3 content,

205

which was 3.65-, 3.17-, 3.03-, and 1.71-fold higher than that in the control fruit on

206

days 3, 7, 14, and 21, respectively (P < 0.05). In the SA-treated fruit, the increased

207

GA3 levels might contribute to alleviating chilling symptoms. GA biosynthetic gene

208

GA3ox1 and catabolic gene GA2ox1 hold the key to bioactive GA levels in higher

209

plants.26 GA homeostasis is maintained through a negative feedback regulation of GA

210

anabolism and a positive feedback regulation of GA catabolism.26,27 Low temperature


Page 10 of 33

Page 11 of 33


211

disrupts GA homeostasis in postharvest tomato fruit mainly through suppressing the

212

gene expression of GA3ox1.16 The present data showed that the GA3ox1 expression

213

patterns in both the control and the SA-treated fruit closely paralleled the fluctuations

214

of GA3 levels (Figure 2B). A high positive correlation was found between GA3ox1

215

gene expression and GA3 content in both the control and the SA-treated fruit with

216

Pearson’s coefficients of 0.90 and 0.88 (P < 0.01), respectively (Figure 2C). It

217

suggested that the exogenous application of SA stimulated GA biosynthesis through

218

upregulating the transcript levels of GA3ox1 in tomato fruit during cold storage.

219

Likewise, Lee and Park19 also reported that SA could promote the seed germination of

220

Arabidopsis under high salinity by inducing the gene expression of GA3ox1.

221

Effect of SA on GAI gene expression in tomato fruit during storage at 4 °C.

222

Key components of the GA signaling pathway are the nuclear-localized DELLA

223

proteins.28 DELLA proteins are plant growth repressors whose degradation is

224

promoted by GA.29 GAI gene expression in the control fruit increased and reached a

225

peak on day 14, and then decreased gradually. In the SA-treated fruit, the transcript

226

levels of GAI were 50%, 44%, 30%, and 22% lower than those in the control fruit on

227

days 3, 7, 14, and 21, respectively (P < 0.05) (Figure 3A). The GAI gene expression

228

was negatively correlated with the GA3 levels in both the control and the SA-treated

229

fruit with Pearson’s coefficients of 0.85 and 0.61 (P < 0.01), respectively (Figure 3B).

230

The present results revealed that SA application stimulated GA biosynthesis, and then

231

downregulated GAI expression in postharvest tomato fruit during long-term cold

232

storage.



233

Effect of SA on gene expression of CBF1 and GA2ox1 in tomato fruit during

234

storage at 4 °C. The transcript levels of cold-responsive gene CBF1 in the control

235

fruit increased gradually from day 3 through day 14, and decreased sharply afterward

236

(P < 0.05; Figure 4A). Compared with the control, the SA-treated fruit exhibited

237

higher levels of CBF1 expression at the corresponding time points. The data were

238

supported by the findings of Dong et al.,30 suggesting that exogenous SA application

239

elevated expression levels of CBF in chilling responses in cucumber seedlings. As

240

shown in Figure 4B, the expression of GA2ox1 in the control fruit reached a

241

maximum on day 14, and then decreased gradually under GA deficiency caused by

242

low temperatures (P < 0.05). In the SA-treated fruit, the transcript levels of GA2ox1

243

were upregulated, which were 1.73-, 1.64-, 1.60-, and 1.56-fold higher than those in

244

the control fruit, respectively (P < 0.05). The present study suggested that the positive

245

feedback regulation in chilled tomato responded normally to the increased GA3

246

content induced by exogenous SA application. In addition, the CBF1 expression

247

patterns (Figure 4A) roughly mirrored the observed variation of GA2ox1 expression

248

(Figure 4B). A positive correlation was found between CBF1 and GA2ox1 expression

249

patterns in both the control and the SA-treated fruit with Pearson’s coefficients of 0.67

250

and 0.88 (P < 0.01), respectively (Figure 4C). It is indicated that CBF1 participated in

251

SA-modulated chilling tolerance and regulated the expression of GA2ox1. This result

252

was consistent with previous studies,28,31-33 which indicated that CBF modulated GA

253

catabolism via the induction of GA2ox genes in Arabidopsis, tobacco and soybean

254

plants under abiotic stresses.


Page 12 of 33

Page 13 of 33


255

Effect of SA on ROS production and antioxidant enzyme activities in tomato

256

fruit during storage at 4 °C. Oxidative stress, that is the excess production of ROS

257

including O2•− and H2O2, has been reported to be associated with the CI development

258

of postharvest fruit.34 In the present study, the O2•− production rate in the control fruit

259

increased gradually throughout the storage period (P < 0.05; Figure 5A). SA

260

treatment significantly reduced the O2•−production rate in the treated fruit, which were

261

12%, 10%, 8%, and 5% lower than that in the control fruit (P < 0.05). The H2O2

262

content in the control fruit showed a remarkable increase, while the H2O2 content in

263

the SA-treated fruit was significantly lower than that in the control fruit (P < 0.05;

264

Figure 5B). These results indicated that the exogenous application of SA inhibited

265

ROS overproduction and alleviated ROS-mediated oxidative damages resulting in CI

266

in tomato fruit under chilling stress, which is consistent with the studies reporting that

267

SA treatment reduced endogenous levels of ROS in lemon flavedo35 and peach fruit36

268

during cold storage.

269

The antioxidant enzyme system plays a critical role in ROS scavenging to protect

270

cell membranes, which is thought to be a major mechanism of resistance to chilling

271

stress.37,38 As shown in Figure 5C, the SOD activity in the control fruit increased

272

gradually during the early storage period. SA treatment slightly but significantly

273

induced the SOD activity, which was 1.21-, 1.13-, 1.12-, and 1.08-fold higher than

274

that in the control fruit on days 3, 7, 14, and 21, respectively (P < 0.05). The CAT

275

activity in the control fruit reached a maximum on day 14, and then declined sharply

276

(Figure 5D). In the SA-treated fruit, the CAT activity showed the same trend as the



277

control but was significantly higher from day 3 through day 14 (P < 0.05). It has been

278

shown that SOD can catalyze the dismutation of O2•− to H2O2, and H2O2 can be

279

scavenged by CAT.34,38 In this study, less ROS accumulation in the SA-treated fruit

280

was attributed to increased activities of SOD and CAT during early stages of cold

281

storage. A recent study reported that the overexpression of PmhCBFc in Arabidopsis

282

improved freezing- and oxidative-stress tolerance, and the SOD activity was elevated

283

in the transgenic Arabidopsis during freezing–thawing cycles.39 Hsieh et al.40 pointed

284

out that the enhancement of chilling tolerance in transgenic tomato overexpressing

285

CBF1 may be due to the induction of the CAT1 gene expression and its enzyme

286

activity. In the present study, a high positive correlation was also found between

287

CBF1 gene expression and SOD activity, and CAT activity in the control and the

288

SA-treated fruit with Pearson’s coefficients of 0.91 and 0.88, and 0.59 and 0.71 (P

Salicylic-Acid-Induced Chilling- and Oxidative-Stress Tolerance in

Recommend Documents