MeJA promotes phospholipid remodeling and jasmonic acid signaling

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Omics Technologies Applied to Agriculture and Food

MeJA promotes phospholipid remodeling and jasmonic acid signaling to alleviate chilling injury in peach fruit Mengshuang Chen, Huimin Guo, Shuqi Chen, Tingting Li, Meiqing Li, Arif Rashid, Changjie Xu, and Ke Wang J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.9b03853 • Publication Date (Web): 16 Aug 2019 Downloaded from pubs.acs.org on August 19, 2019

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Journal of Agricultural and Food Chemistry

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MeJA promotes phospholipid remodeling and jasmonic acid

2

signaling to alleviate chilling injury in peach fruit

3 4

Mengshuang Chen1, Huimin Guo2, Shuqi Chen1, Tingting Li1, Meiqing Li1, Arif

5

Rashid3, Changjie Xu4, Ke Wang1*

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1

8

University, Hefei 230036, China

9

2

Anhui Engineering Laboratory for Agro-products Processing, Anhui Agricultural

Center for Biological Technology, Anhui Agricultural University, Hefei 230036,

10

China

11

3

School of Life Science, Anhui Agricultural University, Hefei 230036, China

12

4

College of Agriculture and Biotechnology/Zhejiang Provincial Key Laboratory of

13

Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus,

14

Hangzhou 310058, China

15 16 17

* Corresponding author：

18

Dr. Ke Wang (E-mail: [email protected])

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ACS Paragon Plus Environment


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ABSTRACT

21

Chilling injury (CI) is a physiological disorder induced by cold, which heavily limit

22

crops production and postharvest preservation worldwide. MeJA can alleviate CI in

23

various fruit species, including peach; however underlying molecular mechanism is

24

poorly understood. Here, changes in contents of phenolics, lipids, and jasmonic acid

25

(JA), and gene expressions, are compared between MeJA and control fruit. Exogenous

26

MeJA inhibited expressions of PpPAL1, PpPPO1 and PpPOD1/2, but did not affect

27

phenolics content. Furthermore, MeJA fruit showed lower relative electrolyte leakage,

28

indicating less membrane damage. Meanwhile, the enrichment of linoleic acid in the

29

potential lipid biomarkers, especially PC, PE and PG, coincided with lower

30

expressions of PpFAD8.1, but higher PpLOX3.1, and JA content. In the JA signaling

31

pathway, MeJA significantly upregulated expressions of PpMYC2.2 and PpCBF3, but

32

downregulated PpMYC2.1. In conclusion, adjustments of fatty acids in phospholipids

33

contribute to MeJA-induced alleviation of CI in peach fruit, via induction of JA

34

mediated CBF pathway.

35 36 37 38

KEYWORDS: Peach, MeJA, chilling injury, fatty acids, lipid

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INTRODUCTION

41

For horticultural products of typical crop categories, cold storage is often used to

42

prolong their postharvest life, whereas long-term storage will cause a series of

43

physiological disorders termed chilling injury (CI), especially for certain tropical and

44

subtropical fruit and vegetables 1. Therefore, the elucidation for CI is of great

45

economic importance and has become a hot scientific issue to be addressed globally

46

during recent decades. Similar microscopic changes were observed during CI of

47

different horticultural products, while macroscopic changes were quite different, such

48

as abnormal skin colors, woolliness 2 and lignin development 3-5, surface and internal

49

browning (IB) 6-10.

50

IB is one of classic CI symptoms, and has often been considered as a visible

51

maker to reflect the CI intensity 11. The occurrence of IB is mainly facilitated by three

52

factors, including phenolic substrates, relative enzymes, including phenylalanine

53

ammonialyase (PAL), polyphenol oxidase (PPO) and peroxidase (POD), as well as

54

their compartmentalization by membrane as barriers 12. The function and integrity are

55

crucial for the compartmentalization of membrane, and it has been reported that

56

membrane lipids have a close impact on the function and integrity of the membranes.

57

Based on their structure and content difference, membrane lipids are generally divided

58

into glycerolipids and sphingolipids. The unsaturated level of total fatty acids (FAs)

59

was found to be positively correlated with chilling tolerance of many fruit species

60

under cold conditions 13-16. In addition, based on lipidome technique, the types of lipid

61

molecular species associated with chilling tolerance have recently been identified in

62

the plants

63

and fatty acids (FAs) have been identified, such as FA desaturase (FAD), and

17-19

and fruit

7, 20

. Meanwhile, many enzymes leading to changes to lipids



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lipoxygenase (LOX), involved in desaturation of FAs and peroxidation, respectively.

65

It is reported that these two enzymes are closely associated with CI 21-23.

66

Among diverse strategies against CI, phytohormone treatments often confer

67

effects of CI alleviation and quality on extensive range of horticultural products,

68

including ethylene

69

brassinosteroids 29-30, salicylic acid

70

that CI was ameliorated by JA exogenous donor MeJA in kinds of horticultural

71

products, including loquat fruit 34-35, orange fruit 36, pomegranate fruit 37, tomato fruit

72

22, 38-39

73

significant CI tolerance in diverse horticultural products, its economic and applicable

74

characteristics make it become a promising postharvest strategy for their quality

75

control.

24

, abscisic acid 31-33

25

, gibberellin acid

26-27

, melatonin

22, 28

,

, and jasmonic acid (JA). It has been reported

, papaya fruit 40-41, banana peel 41, kiwifruit 42, peach fruit 43-45. In addition to its

76

The mechanism of MeJA conferring CI resistance has been extensively studied. It

77

has been reported that JA biosynthesis and its signaling transduction pathway have an

78

effect on chilling tolerance

79

from release of unsaturated FAs from membrane lipids and further catalyzed by a

80

series of enzymes including LOX, allene oxide synthase, allene oxide cyclase,

81

cis-(+)-12-oxo-phyto-dienoic acid reductase. In addition, antioxidant systems

82

shock proteins 46, crytoprotectants 38, 44, energy substances and membrane lipids 43, are

83

reported to be part of effects of MeJA on chilling tolerance. Furthermore, the cascades

84

of C-repeat-binding factors (CBFs) couple with its inducer of CBF expression (ICE),

85

has been proved to be linked with the response induced by MeJA through interaction

86

between their corresponding key transcription factor ICE1 and MYC2 in banana fruit

87

41

39, 41

. The biosynthesis of the endogenous JA originates

.


35

, heat

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Although the understanding of chilling tolerance induced by MeJA has been

89

greatly expanded in past decades, the mechanism of MeJA on IB alleviation shared by

90

many horticultural products is still controversial. For phenolic content, some studies

91

showed negative effects of MeJA 37, 45, whereas others were positive

92

membrane barrier, MeJA could inhibit membrane damage, and maintain a high ratio

93

between unsaturated FAs and saturated FAs 43, however, the details of membrane lipid

94

reprogramming, and key genes remain to be elucidated. Peach is a typical climacteric

95

fruit with short shelf life of often less than one week. Cold storage can cause a variety

96

of CI symptoms such as woolliness, loss of juice, volatiles and ability to ripen, as well

97

as IB. It has been reported that peach IB can be alleviated by MeJA, and phenolics

98

metabolism has been investigated at physical and biochemical level, however

99

underlying molecular mechanism is not fully understood, and lipidome adjustments

100

47-48

. In term of

by MeJA remains to be uncovered.

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‘Xiazhimeng’ is among stony-hard peaches and shows high chilling sensitiveness

102

according to our preliminary studies. This study aims to provide more insights into

103

lipid reprogramming involved in CI alleviated by MeJA. The results are helpful to

104

understand the cold tolerance mechanism conferred by MeJA, and the technological

105

innovation of CI prevention and amelioration for horticultural products.

106 107

MATERIALS AND METHODS

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Plant Materials and Treatments

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Peach (Prunus persica Batsch cv. Xiazhimeng) fruit were harvested at commercial

110

maturity from an orchard in Hefei, Anhui, China, and were transferred to the

111

laboratory once harvest. The uniform fruit without visual defects were randomly

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divided into two groups. One group of fruit were fumigated among 10 μmol L-1 MeJA



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(Sigma-Aldrich, St. Louis, MO, USA) for 24 h at 20℃. After ventilation for 1 h, the

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fruit were stored at 0℃; the other group of fruit were also held under the same

115

condition as the first group without MeJA fumigation. After 63 days of cold storage,

116

the fruit were transferred to 20℃ for six days to mimic shelf life. The samplings were

117

performed at the end point of shelf life (63+6d). Fifteen fruit were sampled at the

118

sampling point and randomly divided into three biological replicates with ﬁve fruit in

119

each replicate. The mesocarp was sliced and immediately frozen in liquid nitrogen

120

and stored at −80°C for further analysis.

121

Internal browning index and electrolyte leakage rate

122

An IB index was calculated to evaluate the degree of ﬂesh browning based on a

123

previous study 7. Electrolyte leakage rate was determined as described by Wang 49.

124

Transcriptomic analysis and real-time quantitative PCR

125

The RNA samples of peach mesocarp were sent to commercial company (Personal

126

Biotechnology Co., Ltd, Shanghai City, China) for transcriptome sequencing. Briefly,

127

total RNA of mesocarp tissues of peach fruit were extracted using kit of TRIzol

128

(Ambion, Austin, USA). Reads were filtrated by three steps of removing adaptor

129

sequences, low quality (< Q20) and length shorter than 50bp, followed by quality

130

checking with FastQC (version 0.11.6). The clean reads were then aligned to the

131

peach genome (V2.1) by bowtie/tophat2. Gene-level raw read counts were normalized

132

using transcript per million (TPM) by Stringtie (version 1.33).

133

Real-time quantitative PCR was performed as described by Wang 49. The primers

134

information is listed in the Table S1.

135

Lipid extraction

136 137

Lipid extraction was conducted followed by the reported method

20

with minor

modifications. Mesocarp of peach (n = 5) were ground to power under liquid nitrogen,


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and 25 mg of powder were weighed for further lipid extraction. 1 mL of methanol:

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methyl tertbutyl ether: water (1:3:1) mixtures were prepared and mixed with the

140

sample for 20 min at 4℃; after addition of water: methanol (3:1) mixture, lipophilic

141

phase were collected, and dried with high purity nitrogen. The dried lipid extracts was

142

recovered in buffer B (in the section of lipidome analysis) and further purified

143

through 0.22 μm syringe filter.

144

Lipidome Analysis

145

One microliter of samples was injected on a Waters ACQUITY UPLC BEH C8

146

column (100 mm × 2.1 mm, 1.7 μm, Waters, USA) connected with guard column, on

147

platform of a Thermo Scientific UHPLC system and coupled with Q Exactive mass

148

spectrometer (Thermo Fisher Scientific, Bremen, Germany). The two mobile phases

149

were water with 0.1% acetic acid (phase A), and acetonitrile with 0.1% acetic acid

150

(phase B), respectively. The gradient separation conditions were as follows: flow rate

151

of 0.3 mL min-1. 1 min phase A, and then 5 min linear gradient from 100% to 50%

152

before 24 min linear gradient from 50% to 0%. The phase A was recovered to 100%

153

and re-equilibrated for 4 min before next injection.

154

The mass analysis was conducted under both positive and negative ion modes. For

155

positive ion mode, the full MS scan type range from 70 m/z to 1050 m/z; resolution

156

70000, sheath gas flow rate 45, aux gas flow rate 15 arb, sweep gas flow rate 1 arb,

157

spray voltage 3.8 KV, capillary temperature 350℃, S-lens RF level of 60, aux gas

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heater temperature 350℃; and for the negative ion mode, full MS scan type range

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from 100 m/z to 1500 m/z; resolution 70000, sheath gas flow rate 40 arb, aux gas flow

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rate 10 arb, sweep gas flow rate 0, spray voltage 3.1 KV, capillary temperature 320℃,

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S-lens RF level of 60, aux gas heater temperature 350℃.

162

Chromatograms peak detection, integration and alignment across samples were



163

performed using LipidsearchTM software (version 4.1, Thermo Fisher Scientific,

164

Germany).

165

Jasmonic acid determination

166

Two hundred micrograms of sample powder were weighed for JA extraction. The

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1.5 mL extraction buffer (methanol: water: formic acid = 7.9: 2: 0.1) was mixed with

168

the sample. After ultrasonication for 30 min on ice, the mixtures were incubated at 4℃

169

for 12 h, and centrifuged (13000×g) for 20 min at 4℃. The supernatants were

170

decanted to new tubes and the remaining fruit tissue was retracted followed by above

171

manipulations. The twice supernatants were collected with first one, and enriched

172

through MAX SPE column (60mg, 3mL, Waters, USA). The final elution was dried to

173

powders with high purity nitrogen and recovered with solvent (acetonitrile: formic

174

acid: water = 5: 0.1: 94.9).

175

JA detection were performed on ACQUITY UPLC H-Class platform (Waters,

176

USA) through Waters ACQUITY UPLC HSS T3（100 * 2.1 mm, 1.7 μm, Waters,

177

USA）, with 1.0 μl volume of injection. Two-phase wash buffer consisted of phase A

178

(0.1% formic acid in water) and phase B (0.1% formic acid in acetonitrile). Gradient

179

separation program was as following: after equilibrium at 95% phase A, 1 min linear

180

gradient from 95% to 30%, then constant for 1 min; recovered to 95% and kept

181

equilibrium for 1 min before next injection. MassLynx software (version 4.1, Waters,

182

USA) was used for signal extraction and quantification.

183

Statistics analysis

184

The Experiment was designed based on random principles; variance analysis via

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Student T-test method was conducted with Microsoft Excel and OPLS-DA was

186

performed by ‘ropls’ package on R.

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RESULTS

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Effect of MeJA on internal browning and phenolic metabolism of peach fruit

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IB index and relative electrolyte leakage rate of MeJA-treated fruit was

191

significantly 50% and 20% lower, respectively, than that of control fruit at the end of

192

shelf life (63 days of cold storage at 0℃ plus 6 days at 20℃, Fig. 1), suggesting that

193

MeJA could significantly inhibit CI-induced IB and cellular membrane permeability

194

in ‘Xiazhimeng’ peach fruit.

195

In order to examine expression of genes related to IB, transcriptomic data in the

196

samples was obtained and validated by real-time quantitative PCR (Fig S1). In

197

comparison with control fruit, significantly lower transcript levels of PpPPO1 and

198

PpPOD1/2 involved in phenolic depletion were observed in MeJA fruit (Fig 2A).

199

Similarly, PpPAL1 involved in phenolic biosynthesis exhibited significantly lower

200

transcript levels. However, no significant differences were observed in the content of

201

total phenolics between MeJA and control fruit (Fig S2).

202 203

Untargeted lipidome reprogramming in peach fruit

204

Since the changes of phenolics cannot fully explain the less IB in MeJA fruit,

205

whereas membrane permeability was significantly inhibited by MeJA, further

206

membrane lipid reprogramming was evaluated. In order to investigate adjustments of

207

membrane lipids, an untargeted lipidomic analysis platform for peach fruit was

208

developed, and 56 lipid species were identified (Table. 1). Phosphatidylcholines (PCs,

209

nine species) and phosphatidylethanolamines (PEs, nine species) in phospholipids

210

were the most abundant lipid species after alignment across samples in this study. In

211

addition, sphingolipids including glycosylceramide (GCer) and ceramide (Cer) were



212

identified. These findings indicate that our system is suitable for the investigation of

213

polar glycerolipids and partial sphingolipids.

214

Several lipid species including two PCs and three PEs, and two (PGs), one Cer

215

and one (TG) were found to be significantly differentially accumulated between

216

MeJA and control fruit (Table. 1). The contents of total PEs and PGs, showed higher

217

levels in MeJA fruit relative to control fruit (Fig 3A). Although no considerable

218

changes in levels of total PCs, two species of PCs showed significant difference in

219

MeJA relative to control, including PC (18:2/18:2), PC (16:0/18:2) with higher levels

220

(Fig 3B). Besides, PE (16:0/18:2), PE (18:0/18:2), PE (18:2/18:2), PG (16:0/18:1),

221

PG (16:0/18:2) and PI (16:0/18:2), exhibited higher accumulation, as well.

222

In order to filter out lipid species contributing to separation of MeJA fruit from

223

control fruit, an orthogonal partial least squares-discriminant analysis (OPLS-DA)

224

model was established. It is well fitted (R2X = 0.935) and predictively (Q2Y = 0.975),

225

and there is clear divergence between MeJA and control fruit in the OPLS-DA score

226

plot (Fig 4A). Variable importance of projection (VIP) represents a summary vector

227

that explains the total importance of variances in the model. A clear negative

228

correlation between VIP and Student t-test P-value was observed, and three PCs

229

(18:0/18:2, 18:2/18:2, 16:0/18:2), two PEs (18:0/18:2, 18:2/18:2), PG (16:0/18:1), Cer

230

(d16:0/2:0) and FA (20:1) were of both high VIP (> 1) and low P-value (< 0.05, Fig

231

4B), indicating potential biomarkers for MeJA fruit during CI development after

232

long-term cold storage.

233 234

Changes of unsaturation status in fatty acid acyls in differentially accumulated

235

lipid molecular species


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Intriguingly, with exception of linolenic acid (18:3), all FA acyl chains especially

237

linoleic acid (18:2) in potential phospholipid biomarkers, especially PC, PE and PG,

238

showed higher levels (approximately two-fold higher) in MeJA fruit, compared with

239

control fruit (Fig 4C), indicating significant effects of MeJA on unsaturation of FA in

240

phospholipids. Therefore, transcript encoding enzymes involved in FA metabolism

241

were studied based on transcriptomic data. Five genes encoding FAD and three ones

242

encoding LOX displayed differential expression between MeJA fruit and control fruit

243

(Fig 5, 6). Although no significant differences in transcript levels of PpFAD2 in MeJA

244

fruit, significantly lower transcript levels of PpFAD6 and PpFAD8s were observed

245

relative to control fruit, especially PpFAD8.1 (Prupe.6G056100) being approximately

246

4.7-fold lower (Fig 5A). Additionally, PpFAD8.1 presented second highest mRNA

247

abundance among PpFADs. One putative PpLOX3 (Prupe.4g047800, designated

248

PpLOX3.1) in MeJA fruit accumulated 10-fold higher transcript levels than control

249

fruit, whereas PpLOX1, lower (Fig 5B).

250

Unsaturated FAs substrate for the JA biosynthesis, and hence JA level was also

251

detected, and MeJA fruit exhibited significantly 46% higher (p=0.013) levels of that

252

relative to control fruit (Fig 6A). The downstream effector of JA signaling, MYC2,

253

putatively encoded by PpMYC2.1 and PpMYC2.2, exhibited significantly 0.6-fold

254

lower (p=0.036) and 7.3-fold higher (p=0.038) transcript levels in MeJA fruit

255

compared with control fruit (Fig 6B-C).

256

To find associations between JA signals and CBFs, which were considered as key

257

factors in acquirement of chilling tolerance in plants, the differentially expressed

258

PpCBFs were examined. One putative PpCBF3 (Prupe.2G289500) showed

259

significantly 13.38-fold higher (p=0.0063) transcript levels in MeJA fruit relative to

260

control fruit (Fig 6D).



261

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DISCUSSION

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Recently IB in peach fruit has involved phenolics metabolism and membrane lipid

263

reprogramming; however a more holistic understanding of mechanism related to its

264

development and tolerance is still limited. In recent years, an approach of lipidome

265

combined transcriptomic analysis, has been performed and provides new insights into

266

this CI symptom

267

reprogramming and phenolic metabolism existed in IB alleviation by low temperature

268

conditioning 7. However, these findings need to be further validated with other

269

strategies such as MeJA, which showed remarkable amelioration of IB in diverse fruit

270

species, such as banana peel, peach, loquat and mango fruit

271

mechanism of MeJA-induced chilling tolerance, many studies focused on its effects

272

on fruit under cold condition, however less attention was paid on CI of fruit after cold

273

removal. In this study, IB alleviation induced by MeJA were observed in peach fruit at

274

the end of shelf life after cold storage for 63 days (Fig 1A); we further confirm that

275

both phenolics metabolism and lipid reprogramming events are involved in CI

276

alleviation processes, and provide more details to understanding on CI.

7, 18, 20

. According to our previous findings, both membrane lipid

35, 40-41, 48, 50

. As for the

277

Here, we propose a model of IB alleviation by MeJA in peach fruit (Fig 7).

278

Inhibition of phenolics metabolism also contributes to alleviation of IB by MeJA,

279

through down-regulating expression of PpPPO1, PpPOD1/2 and PpPAL1. Membrane

280

damage induced by low temperature, such as 0℃, should be alleviated by both

281

reprogramming of lipid molecular species and activation of chilling tolerance

282

pathways. For lipid reprogramming, MeJA inhibits desaturation of linoleic acid (18:2)

283

through downregulating expression of PpFAD8.1. For chilling tolerance pathway,

284

PpCBF3 in CBF signaling pathway is activated by MeJA with enhancement of


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accumulation of JA mediated by up-regulating expression of PpMYC2.2 and

286

PpLOX3.1, and down-regulating that of PpMYC2.1.

287 288

MeJA inhibits both biosynthesis and depletion of phenolics

289

Cold induced IB mainly depends on browning substance of phenolics, which is

290

controlled by generation of phenolics by PAL, and depletion by combined reactions of

291

POD and PPO 28, 51. In our results, MeJA fruit showed less intensity of IB, which is

292

accompanied by a lower level of phenolic metabolism indicated by lower transcript

293

levels of PpPPO1, PpPOD1/2, and PpPAL1 (Fig 2). The reduction of both

294

biosynthesis and depletion could explain the fact of no significant differences of

295

phenolic content in MeJA fruit, in the comparison with control fruit (Fig S2). The

296

results are different to the observation in ‘Baifeng’ peach fruit that the increase in

297

phenolic content and activities of PAL were observed in fruit during shelf life after

298

cold storage

299

‘Baifeng’ is a melting peach, and ‘Xiazhimeng’, stony-hard type. Indeed, dynamics of

300

phenolics contents is hardly consistent among different fruit species when subjected

301

to CI 29, 53.

52

. The cultivar variations should be considered as one of reasons, as

302 303

Promotion of linoleic acid (18:2) in phospholipids against membrane damage

304

In addition to substrate phenolics and enzymes, membrane damage is another

305

factor affecting browning occurrence of horticultural products caused by cold stress,

306

and it depends on the types of lipid molecular species and unsaturated property of FA

307

acyl chains 7. According to previous results of peach lipidome by Bustamante

308

most dramatically changed lipid belongs to galactolipid between six varieties with

309

differential chilling tolerance. Here, we found that differentially accumulated


20

, the


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310

phospholipids were enriched in the MeJA fruit with less IB (Fig 3B). Interestingly, the

311

potential biomarkers related to MeJA-induced amelioration of IB shared the same

312

lipid class, although with different fatty acyl chains 20.

313

In parallel with occurrence of cold-induced IB at the end of shelf life (Fig 1A),

314

phospholipids mainly including PCs, PEs and PGs, with linoleic acids (18:2) enriched

315

in their acyl chains, were differentially accumulated in the MeJA fruit (Fig 3B). It is

316

reported that PCs, PEs and PGs of phospholipids functioning as main components of

317

membrane systems, were associated with CI in horticultural products including peach

318

fruit

319

acyl chains in phospholipids were closely associated with cold-induced IB in peach

320

fruit 7. Previous studies regarding total FAs suggest that levels of unsaturation of FAs

321

were positively correlated with chilling tolerance in fruit including peach during cold

322

storage

323

maintained by MeJA in avocado fruit with less extent to CI during shelf life ripening

324

after cold storage

325

phospholipids may be the conserved FA adjustment by MeJA at shelf life of peach

326

fruit after cold storage.

7, 20

. In addition, our previous findings suggest that the unsaturation status of FA

13

. Recently, it is reported that higher levels of total linoleic acid (18:2) was

54

. Therefore, maintenance of levels of linoleic acid (18:2) in

327

In addition, MeJA-triggered maintenance levels of linoleic acid (18:2) in

328

phospholipids was accompanied by inhibited membrane permeability as indicated by

329

lower levels of relative electrolyte rate at the end of shelf life e (Fig 1B). Decline of

330

linoleic acid (18:2) and increase of linolenic acid (18:3) in PCs and PEs were often

331

observed concomitant with proceeding membrane leakage at the early stage of banana

332

fruit ripening and senescence 55, which were inhibited by MeJA in peach fruit

333

mentioned above. It is suggested that MeJA-triggered maintenance of levels of


56-57

, as

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334

linoleic acid (18:2) in phospholipids involve less membrane damage of CI-induced

335

ripening and senescence.

336 337

Inhibition of PpFAD8.1 but elevation of PpLOX3.1 expression by MeJA

338

contributes to unsaturation status in phospholipids and JA generation

339

The unsaturation levels of FAs are controlled by synergistic actions of FAD and 21-23

340

LOX

. The elevated accumulation of linoleic acid (18:2) in differentially

341

accumulated phospholipids coincided with lower transcript levels of PpFAD8.1 (Fig

342

4C, Fig. 5A). The similar results were observed in melting peach fruit ‘Hujingmilu’

343

with reduced IB in low temperature conditioning treatment at the end of shelf life 7.

344

PpFAD8.1 is the homologue of Arabidopsis FAD8, which is located in plastid (ω-3)

345

and can convert linoleic acid (18:2) to linolenic acid (18:3). FAD8 in plants is to be

346

considered a functional gene involved in cold stress 58-59. In the peach fruit, PpFAD8.1

347

response to cold stress was enhanced by low temperature conditioning fruit with slight

348

CI 7. Therefore, two distinct actions of PpFAD8.1 may exist in peach fruit when

349

facing different temperature environment.

350

Considering the depletion of unsaturated FAs, we further analyzed the expression

351

of PpLOXs. LOX action was closely related to JA level demonstrated by the fact that

352

linolenic acid (18:3) metabolism were significantly influenced in JA-deficient

353

Arabidopsis mutant after exogenous MeJA treatment

354

genes which can be categorized into 9-LOX and 13-LOX depending on oxygenated

355

site in the hydrocarbon backbone of FA. MeJA promoted PpLOX3.1 accumulation in

356

the transcript level, accompanied by elevated JA levels (Fig. 5B, Fig. 6A).

357 358

60

. It is encoded by multiple

PpLOX3.1 putatively belongs to 13-LOX subfamily, and act as the most abundant mRNA member in peach fruit under either cold or normal condition


7, 61

; it is


7, 57, 62

Page 16 of 39

359

responsive to cold stress and MeJA signal in peach fruit

360

tomato TomLOXE was found to be involved in JA biosynthesis to cope with abiotic

361

stress based on transgenic experiment

362

enzymatic activity of PpLOX3.1 were upregulated by exogenous MeJA in peach fruit

363

postharvest ripening

364

such as JA biosynthesis, tolerance to cold stress and fruit ripening. Moreover, there is

365

no linolenic acid (18:3) in the differentially expressed lipids (Fig. 4B-C), support the

366

notion that MeJA accelerated depletion of linolenic acid (18:3) to accumulate

367

endogenous JA via enhancing PpLOX3.1 expression in postharvest ripening after cold

368

storage.

57

63

. Its orthologue in

. Both expression of PpLOX3.1 and

. These data suggest that PpLOX3.1 may play multiple roles

369 370

MeJA promotes downstream CBF signaling pathway through PpMYC2.1

371

expression

372

The enhanced JA level was in parallel with evoked transcript levels of PpMYC2.2,

373

and PpCBF3 in MeJA fruit (Fig 6). MYC2 is a key positive effector of JA signal, and

374

CBF3 cascade has been demonstrated to be one of crucial pathways contributing to

375

cold tolerance in plants and fruit

376

MaMYC2b) physically interacted with ICE1 that can directly transactivate CBF, when

377

expression of downstream genes in CBF signaling cascades were also induced by

378

MeJA treatment 41. Recently, Wang et al. 66 reported that overexpression of MdMYC2

379

in apple calli upregulated MdCBF3 expression and enhanced freezing tolerance.

380

These data suggest that MYC2-related activation of CBF signaling pathway is a

381

general mechanism conferring cold tolerance, which may include PpMYC2.2 and

382

PpCBF3, and further enhanced by endogenous JA accumulation in peach fruit.

64-65

. In banana fruit, MYC2s (MaMYC2a and


Page 17 of 39


383

Further evidence will be needed to provide more insights into roles of PpMYC2s, and

384

associations with PpCBF3 signaling pathway.

385

In this study, details of transcript and metabolites related to phenolics metabolism

386

and lipid reprogramming were investigated to provide insights into CI amelioration by

387

MeJA in peach fruit after cold removal. Phenolics metabolism and phospholipids

388

especially PC, PE and PG were the main influenced factors by MeJA. Moreover,

389

PpFAD8.1 and PpLOX3.1 might control unsaturation status of fatty acid acyls in

390

phospholipids, and JA level. Enhanced JA further activates CBF signaling pathway

391

with participation of PpMYCs, to protect from membrane damage in peach fruit after

392

cold removal.

393 394

ABBREVIATIONS USED

395

CBF: C-repeat-binding factor; Cer: ceramide; CI: chilling injury; FAD: fatty acid

396

desaturase; GCer, glycosylceramides; IB: internal browning; JA: jasmonic acid; LOX:

397

lipoxygenase; MeJA: methyl jasmonate; PAL: phenylalanine ammonialyase; PC:

398

phosphatidylcholine; PE: phosphatidylethanolamine; PG: phosphatidylglycerol; PI:

399

phosphatidylinositol; POD: peroxidase; PPO: phenol oxidase; TG: triacylglycerol..

400 401

Funding

402

This research is supported by Anhui Provincial Department of Education Natural

403

Fund (No. KJ2018A0130), and Natural Science Foundation of Anhui province (No.

404

1808085MC94), and National Natural Science Foundation of China (No. 31772367).

405

AUTHOR INFORMATION



406

Corresponding Author

407

*Dr. Ke Wang Telephone: +86-0551-65785021 E-mail: [email protected]

408 409

ORCID

410

https://orcid.org/0000-0003-3082-4302

411

Notes

412

All authors declare that they have no conflict of interest.

413

Supporting Information

414

Table S1. Information of primers used in real-time quantitative PCR experiment.

415

Figure S1. Relative expressions of genes through real-time quantitative PCR for

416

verification of transcriptomic data.

417

Figure S2. Content of phenolics in peach fruit stored at 0℃ for 63 days and 20℃ 6

418

days of shelf life.

419

ACKNOWLEDGMENTS

420

We thank the staff members at Omics-laboratory of the Biotechnology Center for

421

Anhui Agricultural University in Hefei, China for providing technical support in mass

422

data collection and the other valuable discussions.

423 424

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Figure Captions

647

Fig 1. IB index (A) and electrolyte leakage rate (B) in peach fruit stored at 0℃ for 63

648

days and 6 days shelf life. Asterisks denote significant levels in the comparison

649

between means of MeJA and control (*, p

MeJA promotes phospholipid remodeling and jasmonic acid signaling

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