Next Article in Journal
Multi-Walled Carbon Nanotubes Improve the Development of Chrysanthemum × morifolium (Ramat.) Hemsl. ‘Jinba’ Inflorescences
Next Article in Special Issue
Transcriptomic Database Analysis of Magnesium Transporter (MGT) Gene Family in Pear (Pyrus bretschneideri) Revealed Its Role in Reproductive Stage Development
Previous Article in Journal
Association of Plant-Parasitic Nematodes and Soil Physicochemical Properties in Tomatoes in Turfloop, Limpopo Province, South Africa
Previous Article in Special Issue
Dynamics of Sugars, Organic Acids, Hormones, and Antioxidants in Grape Varieties ‘Italia’ and ‘Bronx Seedless’ during Berry Development and Ripening
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Jasmonate Promotes Ester Aroma Biosynthesis during Nanguo Pears Storage

1
Key Laboratory of Fruit Postharvest Biology, Shenyang 110866, China
2
Key Laboratory of Protected Horticulture, National & Local Joint Engineering Research Center of Northern Horticultural Facilities Design & Application Technology, Shenyang 110866, China
3
College of Horticulture, Shenyang Agricultural University, 120 Dongling Road Shenhe District, Shenyang 110866, China
4
Research Institute of Pomology, Chinese Academy of Agricultural Sciences, Xinghai South Street 98, Xingcheng 125100, China
5
Liaoning Institute of Pomology, Yingkou 115009, China
6
Department of Pharmacognosy, Faculty of Pharmacy, Zagazig University, Zagazig 44519, Egypt
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Submission received: 20 February 2024 / Revised: 24 March 2024 / Accepted: 26 March 2024 / Published: 28 March 2024
(This article belongs to the Special Issue Advances in Physiology Studies in Fruit Development and Ripening)

Abstract

:
Volatile organic compounds (VOCs) have been known to confer the flavor of fruits, characterizing the quality of fruits. Nanguo pear (Pyrus ussuriensis Maxim.) is widely popular among consumers due to its excellent ‘fruity’ aroma derived from ester aroma substances. Jasmonate (JAs) plays an indispensable role in the formation of many qualities in fruit. Therefore, the present study aimed to explore the effect of jasmonate on the VOCs in the Nanguo pear fruit during storage. During storage, the fruits were treated with various concentrations of methyl jasmonate (MeJA) and sodium diethyldithiocarbamate (DIECA, a JAs inhibitor), the inhibitors of JAs biosynthesis. Subsequently, the composition and levels of VOCs in the fruits were determined using GC-MS. The results showed that 100 uM MeJA treatment could promote the accumulation of ester aroma compounds in Nanguo pear fruits, while 100 mM DIECA had the opposite effect. Meantime, MeJA treatment significantly promoted peel degreening, soluble solids content (SSC), fruit softening, and ethylene formation. The RT-qPCR results showed that JAs stimulated the expression of PuAAT1 and repressed the expression of PuCXEs, leading to an increased accumulation of ester aroma compounds. Overall, these results provide a reference for further research on the effect of JAs on fruit aroma.

1. Introduction

Fruit aroma is crucial in determining consumers’ preferences [1,2,3]. The freshly harvested Nanguo pear (Pyrus ussuriensis Maxim.) possesses an attractive light aroma, which reaches the optimal taste period (OTP) after 9 to 12 days of storage at room temperature [4]. So far, around 100 volatile organic compounds (VOCs) have been identified in Nanguo pear, with an esters content of more than 80% of the VOCs during the OTP [5,6,7]. As such, Nanguo pear is often used as a research material for studying the ester aroma of fruit. However, the multiple aroma components and complex biochemical synthesis processes of Nanguo pear have significantly limited further research on enhancing its aroma quality.
Volatile esters in Nanguo pears are important aroma components in assessing the fruit quality. Ester aroma quality formation is significantly related to the lipoxygenase (LOX) pathway [8]. As the primary precursors, linoleic acid and linolenic acid can be transformed into ester aroma under the action of five key enzymes, including LOX, hydroperoxide lyase (HPL), alcohol dehydrogenase (ADH), alcohol acyltransferase (AAT), and carboxylesterase (CXE). This process involves the oxidation of linoleic acid and linolenic acid, catalysis by LOX, and the production of hydroxy fatty acids [6]. These hydroxy fatty acids are then decomposed into acids and aldehydes by HPL [8]. ADH promotes the conversion of aldehydes to their corresponding C6 alcohols. Finally, the alcohol substrate undergoes an esterification reaction with acyl CoA (acyl CoA) under the catalysis of AAT to form esters [9,10]. Meanwhile, the ester aroma substances are decomposed into alcohols under the action of CXE [11,12,13]. AAT and CXE are key enzymes at the end of the LOX pathway [9,13,14,15], which directly catalyze the synthesis and decomposition of ester aroma compounds.
Jasmonate (JAs) is a jasmonic acid (JA), and its methyl ester (MeJA) and isoleucine conjugate (JA-Iie) are a class of fatty acid derivatives, collectively [16]. MeJA is the earliest jasmonate discovered and was identified in frangipani as an aromatic substance [17]. Later, subsequent studies found that MeJA is a natural plant hormone and signaling molecule that participates in regulating various important biological processes [18,19,20,21,22,23,24]. MeJA is widely used due to its rapid uptake by plants, affordable cost, and safety [22,25]. Sodium diethyldithiocarbamate (DIECA), the most commonly used JAs inhibitor [26,27,28], can reduce JAs biosynthesis by inhibiting the octadecane signaling pathway, and then reduce the content of JAs [29]. Previous studies have reported that JAs plays an indispensable role in ethylene production [30,31], pigmentation synthesis [32,33,34], and aroma formation in fruits [35,36]. However, the effects of JAs regulating aroma on Nanguo pears are only partially understood. Considering the salient contribution of volatile compounds to the aroma quality of Nanguo pears, the role of JA in ester aroma formation needs further exploration.
In the present study, the effect of JAs on the aroma characteristics of Nanguo pears was investigated using MeJA and DIECA treatment. The effect of JAs was evaluated by assessing the alterations in fruit storage, the types of volatile compounds, and fluctuations in ester production capacity through the LOX pathway. Furthermore, the ester aroma levels during the storage of Nanguo pears and the expression of its associated genes were investigated. Overall, these findings provide novel perspectives for enhancing the olfactory attributes of Nanguo pears and lay a foundation for future studies on the molecular mechanisms governing the regulation of Nanguo pear ester aroma synthesis through JA.

2. Materials and Methods

2.1. Plant Material and Treatment

Nanguo pears (Pyrus ussuriensis Maxim.) were harvested from the orchard located in Anshan, China, on the commercial harvest day (135 DAFB) in 2022. The fruits were carefully selected to ensure uniformity in terms of size and ripeness. The harvested fruits of Nanguo pear were divided into seven groups with 50 fruits per group as follows: Group 1 was without any treatment as the control group (CK). Group 2 to 4 were sprayed with 50, 100, and 200 μM methyl jasmonate (MeJA), and Group 5 to 7 were sprayed with 10, 50, and 100 mM Sodium diethyldithiocarbamate (DIECA), respectively. The effects of JAs on fruit storage were explored through the above treatments. MeJA was obtained from the Sigma-Aldrich company (catalog no. 392707, Sigma-Aldrich, Saint Louis, MO, USA), and DIECA (catalog no. SD3506, Sigma-Aldrich, Saint Louis, MO, USA) was obtained from Real-Times Biotechnology, Beijing, China. The harvested fruits were stored at 25 °C under 16 h light/8 h dark and 40% relative humidity for 20 days. Sampling of the fruits occurred every 5 days throughout the storage period. At each sampling time point, a minimum of nine fruits from each treatment group was randomly selected and divided into three sets, consisting of three fruits per set. Later, weight loss, soluble solids content (SSC), fruit firmness, and ethylene production were assessed. The fruits were then promptly collected, frozen using liquid nitrogen, and stored at −80 °C for subsequent experiments.

2.2. Determination of Weight Loss, SSC, Firmness, and Ethylene Production

Weight loss during the initial storage period was determined according to the previously reported methods [37]. Five replicates per treatment (3 fruits per replicate) were used for measurement at 5-day intervals. Weight loss was calculated using the following equation: Weight loss (%) = (Wi − Wf)/Wi × 100, where Wi represents the initial weight of the sample and Wf represents the final weight of the sample.
SSC was determined using a digital refractometer (PAL-13810, Otago, and Tokyo, Japan), and the values were converted to the SSC results and expressed as a percentage (%).
The fruit firmness was determined according to the previously reported method [38]. The skin on each side of the fruit was cut, forming 1 cm diameter incisions. Subsequently, the probe was gently pressed onto the surface of the cut to a depth of 8–9 mm. The firmness of the fruit was determined by the average value of these measurements. This process was repeated on three different fruits as biological replicates to ensure accuracy, and the recorded results can be expressed in Newton (N).
For ethylene production analysis, the samples were collected at regular intervals. Three fruits were placed in an airtight container (0.86 L) for 1 h. Afterward, a 1 mL gas sample was collected using a 1 mL syringe and analyzed using a gas chromatograph (7890A, Agilent Technology, Santa Clara, CA, USA), following the previously described method [30]. For each sampling time, a minimum of nine fruits were used for measurement.

2.3. Extraction and Determination of Volatile Esters

The volatile compounds were extracted and detected according to the previously reported method [4]. The samples frozen at −80 °C are small fruit pieces of Nanguo pear. After the refrigerated sample was ground into a powder, the aroma substances were immediately extracted by headspace solid-phase microextraction (HS-SPME). The extraction process involved using 4 mL of pear juice and 1.5 g of NaCl in a 20 mL vial. Take 1.0 g fruit frozen powder of Nanguo pear, put it in a 15 mL headspace bottle, add distilled water, 1.5 g NaCl, and 1.5 µL 3-octanol (1.2 mg mL−1), preheat it at a constant temperature, stirring at 50 °C; 5 min later, insert 65 µm Solid-phase microextraction (PDMS) fiber (catalog no. 557327-U, SUPELCO, Bellefonte, PA, USA) into the headspace bottle, and then, slowly extract the extraction fiber, so that the fiber end is 1 cm higher than the liquid level. Extraction at 50 °C for 42 min. After the extraction, the extracted fibers were withdrawn and immediately driven into the gas chromatography (7890A, Agilent Technology, Santa Clara, CA, USA)-mass spectrometry (5975C, Agilent Technology, Santa Clara, CA, USA) (GC-MS) inlet. The extracted fibers were analyzed at 250 °C for 5 min.
The GC conditions were as follows: The column was VF-WAXms (CP9205, Agilent Technology, Agilent Technology, Santa Clara, CA, USA). The determination procedure was set at 40 °C for 2 min, 2 °C min−1 for 60 °C, 2 min, 1 °C min−1 for 63 °C, 4 °C min−1 for 71 °C, 1 °C min−1 for 75 °C, and 10 °C min−1 for 135 °C. The temperature was raised to 151 °C at 2 °C min−1 for 1 min, and to 211 °C at 10 °C min−1 for 2 min. Helium is used as the carrier gas and the flow rate is set to 1.1 mL min−1 without diverting.
The MS conditions are set as follows: ion source 230 °C, quadrupole 180 °C, scanning range m/z 30–500 amu, and GC-MS transmission line temperature 250 °C.
Data processing: Qualitative analysis was carried out by searching the NIST II standard spectrum library and the retention time of standards. 3-octanol was used as the internal standard, and the relative content of each aroma substance was calculated by the internal standard method.

2.4. RNA Extraction and Gene Expression Analysis

The total RNA extraction, cDNA synthesis, and quantitative real-time polymerase chain reaction (RT-qPCR) assays were conducted according to the previously reported methods [30]. The primers used in the present study are listed in Supplementary Table S1. PuActin was used as an internal control to ensure standardization.

2.5. Statistical Analysis

The above data were analyzed using SPSS v17.0 (v17.0, SPSS Inc., Chicago, IL, USA), and the results were presented as mean ± SE. The statistical significance difference between two groups of data was determined through the student’s t-test. p-values less than 0.05 (*) and 0.01 (**) were considered significant.

3. Results

3.1. Effects of JAs on Morphology, Weight Loss, and Soluble Solids Content in Postharvest Pear Fruit

In the present study, Nanguo pears (Pyrus ussuriensis Maxim.) were harvested 135 days after full bloom (DAFB) and treated with 50, 100, and 200 μM MeJA and 10, 50, and 100 mM DIECA (a JAs inhibitor) to investigate the role of JAs on the storage of Nanguo pears. Additionally, the morphology, weight loss, and SSC of the fruits were assessed separately using different treatments. The MeJA-treated fruits exhibited a significantly more intense yellow color than the control group (CK). Conversely, the fruits treated with DIECA displayed a visibly greener shade compared to CK, particularly 10 days after harvest (DAH) (Figure 1A). Moreover, MeJA treatment decreased fruit weight during storage, while the application of DIECA prevented weight loss (Figure 1B). SSC gradually increased during fruit storage, and the increase was especially obvious on 5 DAH and 10 DAH (Figure 1C). Compared with the CK, up to 10 DAH, SSC increased by 10.28% and 7.71% under 100 and 200 μM MeJA treatments, respectively, while it decreased by 3.5% and 6.54% under 100 and 200 μM in DIECA-treated pears (Figure 1C). Therefore, we observed that the treatment of fruit with 50 and 100 μM MeJA significantly promoted fruit peel degreening, increased weight loss rate, and elevated SSC, while 50 and 10 µM DIECA had the opposite effect. Among them, 100 µM MeJA and 100 mM DIECA had the most significant effects.

3.2. Effects of JAs Treatment on Firmness and Ethylene Production

During storage, MeJA decreased the firmness of pears, while DIECA delayed the decrease in firmness (Figure 2A). Up to 15 DAH, 100 and 200 μM MeJA treatments decreased the firmness by 42% and 24.56%, respectively, while there was an increase in the firmness in 50 and 100 mM DIECA-treated fruit by 10.13% and 27.55%, respectively, compared with the CK (Figure 2A).
The CK exhibited an increased ethylene production as ripening progressed up until 10 DAH. Conversely, ethylene production in fruits treated with 50, 100, and 200 μM MeJA exhibited a significant elevation (p < 0.01) of 6%, 27.33%, and 10.64%, correspondingly, at the 10 DAH mark compared with the CK (Figure 2B). However, the 50 and 100 mM DIECA treatments had the opposite effect on these indicators, especially for 100 mM at 10 DAH (Figure 2B). Therefore, it was inferred that JAs could promote the ripening of Nanguo pear fruits, with 100 µM MeJA having the most significant promoting effect and 100 mM DIECA having the most significant inhibitory effect.

3.3. Effect of JAs on the Composition and Content of VOCs during Fruit Storage

The total VOCs content of the CK fruit continued to increase during storage, which began to increase at 5 DAH and reached the highest value of 8.36 μg g−1 at 10 DAH and then declined gradually to a low level (Figure 3A). Additionally, 50, 100, and 200 μM MeJA-treated fruits exhibited a further increase by 23.5%, 72.52%, and 21.33%, respectively, at 10 DAH. During storage, DIECA treatment significantly decreased the overall VOC content compared with the CK, especially the 100-millimolar DIECA treatment. It is worth noting that Nanguo pears undergo distinct transformations in terms of aroma compound composition in various stages, which is evident from the shift observed in the volatile composition and the transitioning of aldehydes, acids, and benzenes to esters. MeJA and DIECA treatment had a substantial impact on the content of volatile aroma compounds in Nanguo pears (Figure 3A); however, their effect on the proportion of different volatile compounds was minimal. Notably, in each treatment during the OTP of 10 DAH for Nanguo pear, the highest relative content was found for the ester aroma compounds (Figure 3B).
During storage, a total of 77 volatile compounds were detected through a comprehensive analysis, including 11 aldehydes, 34 esters, 5 ketones, 2 alcohol compounds, 9 terpenoids, 13 benzenes, and 3 acids (Figure 4). Notably, the concentration and diversity of aldehydes decreased over time, whereas the content and variety of esters increased throughout the fruit storage period (Figure 3C and Figure 4). The major compounds at 0 DAH were identified as 2,4-di-t-butylphenol, 3,5-dimethyl benzaldehyde, and trans-2-hexenal, whereas ethyl hexanoate, alpha-farnesene, and ethyl butyrate were dominant at 10 DAH. At 10 DAH, 100 μM MeJA treatment and 100 mM DIECA treatment had the largest effect on the total and relative contents of VOCs (Figure 3). Therefore, this concentration was used in the subsequent experiments.

3.4. Effect of JAs on the Accumulation of Volatile Esters during Fruit Storage

At 10 DAH, the esters in the CK and fruit treated with 100 μM MeJA increased to 14 and 16, respectively. Moreover, the volatile ester compounds in the MeJA-treated samples exhibited a richer variety and higher content compared with the CK samples. However, an opposite effect was observed in the DIECA-treated group, specifically at 10 DAH with a concentration of 100 mM (Figure 4). As shown in Table 1, the aroma profile of Nanguo pear fruit treated with 100 μM MeJA showed ethyl butanoate, ethyl hexanoate, and hexyl acetate as the three dominant esters in terms of both high content and low odor threshold at 10 DAH. The presence of these compounds was verified through gas chromatography-mass spectrometry (GC-MS) analysis at different time points, followed by a comparison between the retention times and standard retention time for ethyl butanoate (5.211 min), ethyl hexanoate (13.279 min), and hexyl acetate (15.602 min) (Figure 5). Subsequently, 100 μM MeJA and 100 mM DIECA were used in the subsequent experiments due to their largest effect on the total and relative contents of VOCs (Figure 3 and Figure 4).

3.5. The Effect of JAs on the Expression of Volatile Esters Accumulation-Related Genes during Fruit Storage

The synthesis of volatile esters in fruits is influenced by two important enzymes, AAT and CXE. As shown in Figure 6, the expression level of PuAAT1 increased in the storage of CK fruits, reaching its peak at 10 DAH and subsequently declining. This trend resembles the pattern observed in the production rate of ethylene. The expression of PuAAT1 was promoted by MeJA and inhibited by DIECA. The catabolism of volatile esters was mainly controlled by PuCXE7, PuCXE15, PuCXE20, and PuCXE25 in Nanguo pear.
In the MeJA-treated and CK pears, the OTP was achieved at 10 DAH. The expression levels of PuCXE7, PuCXE15, PuCXE20, and PuCXE25 were significantly elevated in the DIECA-treated samples compared to the CK (p < 0.05). Moreover, significant differences were observed in the expression pattern of the four genes within the CXE family. At 10 DAH, PuCXE15 exhibited peak levels, which were notably elevated in the DIECA-treated group compared to the CK (p < 0.05). Conversely, MeJA treatment significantly decreased the expression levels of PuCXE7, PuCXE15, PuCXE20, and PuCXE25 during storage (p < 0.05). Additionally, MeJA had a significant impact on the increasing expression of PuAAT1 throughout storage (p < 0.05). Subsequently, the observed rise in volatile esters in the Nanguo pears at 10 DAH can be attributed to the fact that JAs positively regulated the expression of PuAAT1 and negatively regulated the expression of PuCXE7, PuCXE15, PuCXE20, and PuCXE25.

4. Discussion

The sensory quality of fruits greatly depends on their aroma, which is a crucial aspect influencing consumers’ preferences [1,2,3]. So far, more than 2000 kinds of aroma substances, mainly composed of esters, terpenes, aldehydes, alcohols, etc., have been identified in plants [39,40,41]. The composition and content of aroma substances differ in different kinds of fruits. Among them, esters are volatile substances with a ‘fruity’ aroma and low odor threshold, which tend to accumulate more in mature fruits, providing fruits with a characteristic ‘fruity’ aroma in different types and proportions, such as peach (Prunus persica), apple (Malus domestica), and Nanguo pear (Pyrus ussuriensis Maxim.), etc. [9,14,42].
JAs is a naturally occurring plant hormone found in various plant organs, which plays a crucial role in promoting ethylene production, anthocyanin synthesis, and the formation of apple aroma [30,32,36], but the investigations conducted on JAs aroma formation in Nanguo pears during room temperature storage remain incomplete. MeJA is the most widely used jasmonate [20]. Sodium diethyldithiocarbamate (DIECA) can inhibit the JAs pathway by shunting 13(S)-hydroperoxylinolenic acid to 13-hydroxylinolenic, thereby sharply reducing the content of JAs in plants [26]. In the present study, the effect of JAs on Nanguo pears during storage was explored through MeJA and DIECA treatments. The results showed that the Nanguo pear lacks a significant aroma in its newly harvested state. Nevertheless, after 10 days of storage at room temperature, the fully ripened pear attained the optimum taste period (OTP) and released an abundant and captivating fragrance (Figure 4; Table 1). MeJA treatment promoted fruit coloration, fruit softening, SSC formation, and ester aroma accumulation (Figure 1, Figure 2, Figure 3 and Figure 4). However, DIECA treatment had the opposite effect on these indicators (Figure 1, Figure 2, Figure 3 and Figure 4). Additionally, the influences of different treatment concentrations on the parameters mentioned above were investigated. Notably, 100 µM MeJA and 100 mM DIECA treatment had the greatest impact on the total and relative contents of VOCs (Figure 1, Figure 2, Figure 3 and Figure 4). Consequently, these specific concentrations were selected for further experimentation. Such a result provides a reference for further study on the impact of MeJA on the fruit aroma of Nanguo pears.
JAs signaling pathway transcription factor MYC2 plays an active role in regulating various physiological processes. In apples, it was found that MdMYC2 interacted with MdMYB85 to promote the synthesis and accumulation of ester aroma compounds by promoting the expression of MdAAT1, a key gene in the ester aroma synthesis pathway [35]. In navel oranges, CsMYC2 is induced by MeJA treatment, and binds to gene promoters such as CsCCD4b, a key gene in the β-citroulin synthesis pathway, to positively regulate the expression of related genes to promote red skin; DIECA treatment has the opposite effect [32]. In Nanguo pears, JAs also plays a role in promoting fruit ripening, peel chlorosis, and aroma formation (Figure 1, Figure 2, Figure 3 and Figure 6), but the molecular mechanism involved is still unclear.
During storage, the levels of aldehydes experienced a gradual decline, while the levels of esters exhibited a progressive increase [4]. The key aromatic compounds defining the fragrance of ripe Nanguo pears included ethyl butanoate, ethyl hexanoate, and hexyl acetate (Figure 5). Remarkably, these findings were consistent with the previous study results [4,19]. At present, the aroma-related research of Nanguo pears mainly focuses on the extraction and identification of the main aroma components using different storage methods, the analysis of related enzyme activities, and the determination of the genes related to the aroma synthesis pathways [4,43]. Herein, MeJA treatment promoted the accumulation of ester aroma in terms of ester aroma synthesis and catabolism, including promoting the expression of PuAAT1 for ester aroma synthesis and inhibiting the expression of PuCXE7, PuCXE15, PuCXE20, and PuCXE25 for ester aroma catabolism (Figure 6). Nevertheless, additional investigations are required to delve into the mechanisms governing the formation of ester fragrance.

5. Conclusions

In conclusion, MeJA promoted fruit peel degreening, fruit softening, SSC formation, ethylene production, and ester aroma accumulation in Nanguo pears during storage, while DIECA showed the opposite effect. Notably, 100 μM MeJA and 100 mM DIECA treatments are the most effective treatments for promoting and inhibiting the fruit aroma of Nanguo pears, respectively. Additionally, JAs promoted fruit ester aroma accumulation mainly by promoting the gene expression related to ester aroma synthesis and inhibiting the gene expression related to ester aroma catabolism in Nanguo pears. These findings provide a reference for further study on the impact of JAs on the fruit aroma of Nanguo pears.

Supplementary Materials

The following supporting information can be downloaded at https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/horticulturae10040329/s1, Table S1: Primers used in this research.

Author Contributions

Z.Y. conceived and designed the experiments; L.Q., C.L., H.L., J.S., W.L., Y.Y., X.L., Y.D. and I.M. participated in the experiments and data analyses; L.Q. and C.L. wrote the manuscript with inputs and guidance from W.L. and Z.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China (2022YFD2100105), the Natural Science Foundation of Liaoning Province (2022-MS-261), the Research Foundation of the Education Bureau of Liaoning Province (LJKMZ20221025), the General Higher Education Undergraduate Teaching Reform Research Project of Liaoning Province (2022-444), and the Postgraduate Education and Teaching Research Project of Shenyang Agricultural University (2022-yjs-39).

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Klee, H.J.; Tieman, D.M. Genetic challenges of flavor improvement in tomato. Trends Genet. 2013, 29, 257–262. [Google Scholar] [CrossRef]
  2. Tieman, D.; Zhu, G.; Resende, M.F., Jr.; Lin, T.; Nguyen, C.; Bies, D.; Rambla, J.L.; Beltran, K.S.; Taylor, M.; Zhang, B.; et al. A chemical genetic roadmap to improved tomato flavor. Science 2017, 355, 391–394. [Google Scholar] [CrossRef] [PubMed]
  3. Shi, F.; Zhou, X.; Zhou, Q.; Tan, Z.; Yao, M.-m.; Wei, B.-d.; Ji, S.-j. Transcriptome analyses provide new possible mechanisms of aroma ester weakening of ‘Nanguo’ pear after cold storage. Sci. Hortic. 2018, 237, 247–256. [Google Scholar] [CrossRef]
  4. Li, X.; Qi, L.; Zang, N.; Zhao, L.; Sun, Y.; Huang, X.; Wang, H.; Yin, Z.; Wang, A. Integrated metabolome and transcriptome analysis of the regulatory network of volatile ester formation during fruit ripening in pear. Plant Physiol. Biochem. 2022, 185, 80–90. [Google Scholar] [CrossRef] [PubMed]
  5. Wu, X.; Chen, Y.; Wang, X.; Qi, K.; Qiao, X.; Li, Q.; Xie, Z.; Cao, P.; Zhang, S.; Yin, H. New insights into aroma regulation in pear peel and flesh under methyl jasmonate treatment obtained by metabolite and whole-transcriptome RNA sequencing analyses. Postharvest Biol. Technol. 2023, 201, 112347. [Google Scholar] [CrossRef]
  6. Luo, M.; Zhou, X.; Sun, H.; Zhou, Q.; Ge, W.; Sun, Y.; Yao, M.; Ji, S. Insights into profiling of volatile ester and LOX-pathway related gene families accompanying post-harvest ripening of ‘Nanguo’ pears. Food Chem. 2021, 335, 127665. [Google Scholar] [CrossRef]
  7. Schiller, D.; Contreras, C.; Vogt, J.; Dunemann, F.; Defilippi, B.G.; Beaudry, R.; Schwab, W. A dual positional specific lipoxygenase functions in the generation of flavor compounds during climacteric ripening of apple. Hortic. Res. 2015, 2, 15003. [Google Scholar] [CrossRef]
  8. Song, J.; Bangerth, F. Fatty acids as precursors for aroma volatile biosynthesis in pre-climacteric and climacteric apple fruit. Postharvest Biol. Technol. 2003, 30, 113–121. [Google Scholar] [CrossRef]
  9. Li, X.; Gao, S.; Yang, L.; Yin, M.; Li, J.; Zhang, H.; Ji, S. Ethylene promotes ester biosynthesis through PuERF13/PuDof2.5 synergically activated PuAAT1 during ripening of cold-stored ‘Nanguo’ pear. Postharvest Biol. Technol. 2023, 195, 112108. [Google Scholar] [CrossRef]
  10. Morales-Quintana, L.; Moya-León, M.A.; Herrera, R. Computational study enlightens the structural role of the alcohol acyltransferase DFGWG motif. J. Mol. Model. 2015, 21, 216. [Google Scholar] [CrossRef]
  11. Gershater, M.C.; Cummins, I.; Edwards, R. Role of a Carboxylesterase in Herbicide Bioactivation in Arabidopsis thaliana. J. Biol. Chem. 2007, 282, 21460–21466. [Google Scholar] [CrossRef] [PubMed]
  12. Zhang, L.; Zhou, K.; Wang, M.; Li, R.; Dai, X.; Liu, Y.; Jiang, X.; Xia, T.; Gao, L. The Functional Characterization of Carboxylesterases Involved in the Degradation of Volatile Esters Produced in Strawberry Fruits. Int. J. Mol. Sci. 2023, 24, 383. [Google Scholar] [CrossRef] [PubMed]
  13. Martínez-Rivas, F.J.; Blanco-Portales, R.; Moyano, E.; Alseekh, S.; Caballero, J.L.; Schwab, W.; Fernie, A.R.; Muñoz-Blanco, J.; Molina-Hidalgo, F.J. Strawberry fruit FanCXE1 carboxylesterase is involved in the catabolism of volatile esters during the ripening process. Hortic. Res. 2022, 9, uhac095. [Google Scholar] [CrossRef] [PubMed]
  14. Cao, X.M.; Wei, C.Y.; Duan, W.Y.; Gao, Y.; Kuang, J.F.; Liu, M.C.; Chen, K.S.; Klee, H.; Zhang, B. Transcriptional and epigenetic analysis reveals that NAC transcription factors regulate fruit flavor ester biosynthesis. Plant J. 2021, 106, 785–800. [Google Scholar] [CrossRef] [PubMed]
  15. Qi, L.; Li, X.; Zang, N.; Zhang, Z.; Yang, Y.; Du, Y.; Sun, J.; Mostafa, I.; Yin, Z.; Wang, A. Genome-wide identification of CXE and PuCXE15 functions in the catabolism of volatile ester in ‘Nanguo’ pear fruit. Plant Physiol. Biochem. 2023, 203, 107996. [Google Scholar] [CrossRef] [PubMed]
  16. Ruan, J.; Zhou, Y.; Zhou, M.; Yan, J.; Khurshid, M.; Weng, W.; Cheng, J.; Zhang, K. Jasmonic Acid Signaling Pathway in Plants. Int. J. Mol. Sci. 2019, 20, 2479. [Google Scholar] [CrossRef] [PubMed]
  17. Demole, E.; Lederer, E.; Mercier, D. Isolement et détermination de la structure du jasmonate de méthyle, constituant odorant caractéristique de l’essence de jasmin. Helv. Chim. Acta 1962, 45, 675–685. [Google Scholar] [CrossRef]
  18. Wang, M.; Fan, X.; Ding, F. Jasmonate: A Hormone of Primary Importance for Temperature Stress Response in Plants. Plants 2023, 12, 4080. [Google Scholar] [CrossRef] [PubMed]
  19. Min, D.; Li, F.; Ali, M.; Zhang, X.; Liu, Y. Application of methyl jasmonate to control disease of postharvest fruit and vegetables: A Meta-analysis. Postharvest Biol. Technol. 2024, 208, 112667. [Google Scholar] [CrossRef]
  20. Min, D.; Li, F.; Ali, M.; Zhang, X.; Liu, Y. Application of methyl jasmonate to control chilling tolerance of postharvest fruit and vegetables: A meta-analysis and eliciting metabolism review. Crit. Rev. Food Sci. Nutr. 2023, 13, 1–14. [Google Scholar] [CrossRef]
  21. Hickman, R.; Van Verk, M.C.; Van Dijken, A.J.H.; Mendes, M.P.; Vroegop-Vos, I.A.; Caarls, L.; Steenbergen, M.; Van der Nagel, I.; Wesselink, G.J.; Jironkin, A.; et al. Architecture and Dynamics of the Jasmonic Acid Gene Regulatory Network. Plant Cell 2017, 29, 2086–2105. [Google Scholar] [CrossRef]
  22. Scognamiglio, J.; Jones, L.; Letizia, C.S.; Api, A.M. Fragrance material review on methyl jasmonate. Food Chem. Toxicol. 2012, 50, S572–S576. [Google Scholar] [CrossRef] [PubMed]
  23. Rehman, M.; Saeed, M.S.; Fan, X.; Salam, A.; Munir, R.; Yasin, M.U.; Khan, A.R.; Muhammad, S.; Ali, B.; Ali, I.; et al. The Multifaceted Role of Jasmonic Acid in Plant Stress Mitigation: An Overview. Plants 2023, 12, 3982. [Google Scholar] [CrossRef] [PubMed]
  24. Qi, T.; Song, S.; Ren, Q.; Wu, D.; Huang, H.; Chen, Y.; Fan, M.; Peng, W.; Ren, C.; Xie, D. The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana. Plant Cell 2011, 23, 1795–1814. [Google Scholar] [CrossRef] [PubMed]
  25. Fang, H.; Luo, F.; Li, P.; Zhou, Q.; Zhou, X.; Wei, B.; Cheng, S.; Zhou, H.; Ji, S. Potential of jasmonic acid (JA) in accelerating postharvest yellowing of broccoli by promoting its chlorophyll degradation. Food Chem. 2020, 309, 125737. [Google Scholar] [CrossRef] [PubMed]
  26. Li, Y.; Qiu, L.; Zhang, Q.; Zhuansun, X.; Li, H.; Chen, X.; Krugman, T.; Sun, Q.; Xie, C. Exogenous sodium diethyldithiocarbamate, a Jasmonic acid biosynthesis inhibitor, induced resistance to powdery mildew in wheat. Plant Direct 2020, 4, e00212. [Google Scholar] [CrossRef] [PubMed]
  27. Wang, L.; Chen, H.; Chen, G.; Luo, G.; Shen, X.; Ouyang, B.; Bie, Z. Transcription factor SlWRKY50 enhances cold tolerance in tomato by activating the jasmonic acid signaling. Plant Physiol. 2024, 194, 1075–1090. [Google Scholar] [CrossRef] [PubMed]
  28. Wei, X.; Wei, X.; Guan, W.; Nong, W.; Chen, R.; Tao, X.; Mao, L. ABA-responsive transcription factor ABF1-1 promotes JA biosynthesis to accelerate suberin polyphenolic formation in wounded kiwifruit (Actinidia chinensis). Postharvest Biol. Technol. 2022, 187, 111850. [Google Scholar] [CrossRef]
  29. Farmer, E.E.; Caldelari, D.; Pearce, G.; Walker-Simmons, M.K.; Ryan, C.A. Diethyldithiocarbamic Acid Inhibits the Octadecanoid Signaling Pathway for the Wound Induction of Proteinase Inhibitors in Tomato Leaves. Plant Physiol. 1994, 106, 337–342. [Google Scholar] [CrossRef]
  30. Li, T.; Xu, Y.; Zhang, L.; Ji, Y.; Tan, D.; Yuan, H.; Wang, A. The Jasmonate-Activated Transcription Factor MdMYC2 Regulates ETHYLENE RESPONSE FACTOR and Ethylene Biosynthetic Genes to Promote Ethylene Biosynthesis during Apple Fruit Ripening. Plant Cell 2017, 29, 1316–1334. [Google Scholar] [CrossRef]
  31. Song, S.; Qi, T.; Wasternack, C.; Xie, D. Jasmonate signaling and crosstalk with gibberellin and ethylene. Curr. Opin. Plant Biol. 2014, 21, 112–119. [Google Scholar] [CrossRef] [PubMed]
  32. Yue, P.; Jiang, Z.; Sun, Q.; Wei, R.; Yin, Y.; Xie, Z.; Larkin, R.M.; Ye, J.; Chai, L.; Deng, X. Jasmonate Activates a CsMPK6-CsMYC2 module that regulates the expression of β-citraurin biosynthetic genes and fruit coloration in orange (Citrus sinensis). Plant Cell 2023, 35, 1167–1185. [Google Scholar] [CrossRef] [PubMed]
  33. Pei, D.; Ren, Y.; Yu, W.; Zhang, P.; Dong, T.; Jia, H.; Fang, J. The roles of brassinosteroids and methyl jasmonate on postharvest grape by regulating the interaction between VvDWF4 and VvTIFY 5A. Plant Sci. 2023, 336, 111830. [Google Scholar] [CrossRef] [PubMed]
  34. Han, Y.; Chen, C.; Yan, Z.; Li, J.; Wang, Y. The methyl jasmonate accelerates the strawberry fruit ripening process. Sci. Hortic. 2019, 249, 250–256. [Google Scholar] [CrossRef]
  35. Li, L.-X.; Fang, Y.; Li, D.; Zhu, Z.-H.; Zhang, Y.; Tang, Z.-Y.; Li, T.; Chen, X.-S.; Feng, S.-Q. Transcription factors MdMYC2 and MdMYB85 interact with the ester aroma synthesis gene MdAAT1 in apples. Plant Physiol. 2023, 193, 2442–2458. [Google Scholar] [CrossRef] [PubMed]
  36. Liu, X.; Feng, Y.; Li, S.; Li, D.; Yu, J.; Zhao, Z. Jasmonate-induced MdMYC2 improves fruit aroma during storage of ‘Ruixue’ apple based on transcriptomic, metabolic and functional analyses. LWT 2023, 185, 115168. [Google Scholar] [CrossRef]
  37. Zhou, Q.; Ma, C.; Cheng, S.; Wei, B.; Liu, X.; Ji, S. Changes in antioxidative metabolism accompanying pitting development in stored blueberry fruit. Postharvest Biol. Technol. 2014, 88, 88–95. [Google Scholar] [CrossRef]
  38. Zang, N.; Li, X.; Qi, L.; Zhang, Z.; Yang, Y.; Yin, Z.; Wang, A. H2O2-activated transcription factor MdERF4 negatively regulates ethylene biosynthetic during fruit ripening by suppressing MdACS1 transcription. Postharvest Biol. Technol. 2023, 204, 112461. [Google Scholar] [CrossRef]
  39. Li, X.; Gao, P.; Zhang, C.; Xiao, X.; Chen, C.; Song, F. Aroma of peach fruit: A review on aroma volatile compounds and underlying regulatory mechanisms. Int. J. Food Sci. Technol. 2023, 58, 4965–4979. [Google Scholar] [CrossRef]
  40. Li, H.; Liu, G.; Fu, D. Transcriptional regulation of tomato fruit quality. Postharvest Biol. Technol. 2023, 202, 112393. [Google Scholar] [CrossRef]
  41. Li, H.; Ma, C.; Li, S.; Wang, H.; Fang, L.; Feng, J.; Wang, Y.; Li, Z.; Cai, Q.; Geng, X.; et al. Eight Typical Aroma Compounds of ‘Panguxiang’ Pear during Development and Storage Identified via Metabolomic Profiling. Life 2023, 13, 1504. [Google Scholar] [CrossRef] [PubMed]
  42. Souleyre, E.J.F.; Chagné, D.; Chen, X.; Tomes, S.; Turner, R.M.; Wang, M.Y.; Maddumage, R.; Hunt, M.B.; Winz, R.A.; Wiedow, C.; et al. The AAT1 locus is critical for the biosynthesis of esters contributing to ‘ripe apple’ flavour in ‘Royal Gala’ and ‘Granny Smith’ apples. Plant J. 2014, 78, 903–915. [Google Scholar] [CrossRef] [PubMed]
  43. Luo, M.; Zhou, X.; Hao, Y.; Sun, H.; Zhou, Q.; Sun, Y.; Ji, S.-j. Methyl jasmonate pretreatment improves aroma quality of cold-stored ‘Nanguo’ pears by promoting ester biosynthesis. Food Chem. 2021, 338, 127846. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Postharvest MeJA and DIECA treatment affected the fruit peel degreening (scale bar = 2 cm) (A), weight loss (B), and soluble solids content (SSC) (C) of Nanguo pear (Pyrus ussuriensis Maxim.). The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Asterisks indicate statistical differences in treatment compared with the CK (* p < 0.05; ** p < 0.01).
Figure 1. Postharvest MeJA and DIECA treatment affected the fruit peel degreening (scale bar = 2 cm) (A), weight loss (B), and soluble solids content (SSC) (C) of Nanguo pear (Pyrus ussuriensis Maxim.). The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Asterisks indicate statistical differences in treatment compared with the CK (* p < 0.05; ** p < 0.01).
Horticulturae 10 00329 g001
Figure 2. Postharvest MeJA and DIECA treatment affected fruit firmness (A) and ethylene production (B) during Nanguo pear fruit storage. The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Asterisks indicate statistical differences in treatment compared with the CK (* p < 0.05; ** p < 0.01).
Figure 2. Postharvest MeJA and DIECA treatment affected fruit firmness (A) and ethylene production (B) during Nanguo pear fruit storage. The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Asterisks indicate statistical differences in treatment compared with the CK (* p < 0.05; ** p < 0.01).
Horticulturae 10 00329 g002
Figure 3. Effects of MeJA and DIECA treatment on volatile organic compounds (VOCs) of Nanguo pears during fruit storage. (A) Total VOCs contents. The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Asterisks represent statistical differences in treatment compared to the CK (* p < 0.05; ** p < 0.01); (B) relative VOCs content. The different colored columns represent different kinds of volatile substances.
Figure 3. Effects of MeJA and DIECA treatment on volatile organic compounds (VOCs) of Nanguo pears during fruit storage. (A) Total VOCs contents. The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Asterisks represent statistical differences in treatment compared to the CK (* p < 0.05; ** p < 0.01); (B) relative VOCs content. The different colored columns represent different kinds of volatile substances.
Horticulturae 10 00329 g003
Figure 4. Effects of MeJA and DIECA treatment on the VOCs species numbers of Nanguo pears during fruit storage. The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Cuboids, cylinders, pyramids, and cones represent 0, 5, 10, and 15 days after harvest, respectively.
Figure 4. Effects of MeJA and DIECA treatment on the VOCs species numbers of Nanguo pears during fruit storage. The white columns represent untreated fruit as a control group (CK), the yellow columns represent MeJA treatment, and the green columns represent DIECA treatment. Cuboids, cylinders, pyramids, and cones represent 0, 5, 10, and 15 days after harvest, respectively.
Horticulturae 10 00329 g004
Figure 5. GC-MS analysis of three characteristic aroma compounds in a standard solution (A), DIECA treatment Nanguo pear sample (B), CK Nanguo pear sample (C), and MeJA treatment Nanguo pear sample (D) on the 10th day after the harvest of Nanguo pears. The retention times of ethyl butanoate, ethyl hexanoate, and hexyl acetate were approximately 5.211, 13.279, and 15.602 min, respectively.
Figure 5. GC-MS analysis of three characteristic aroma compounds in a standard solution (A), DIECA treatment Nanguo pear sample (B), CK Nanguo pear sample (C), and MeJA treatment Nanguo pear sample (D) on the 10th day after the harvest of Nanguo pears. The retention times of ethyl butanoate, ethyl hexanoate, and hexyl acetate were approximately 5.211, 13.279, and 15.602 min, respectively.
Horticulturae 10 00329 g005
Figure 6. The expression levels of PuAAT and PuCXE genes in Nanguo pears during storage. Relative expression of PuAAT1 (A); PuCXE7 (B); PuCXE15 (C); PuCXE20 (D); PuCXE25 (E). The white lines represent untreated fruit as a control group (CK), the yellow lines represent MeJA treatment, and the green lines represent DIECA treatment. Asterisks represent the significant difference between MeJA or DIECA treatment and the CK. Statistical significance: * p < 0.05, ** p < 0.01.
Figure 6. The expression levels of PuAAT and PuCXE genes in Nanguo pears during storage. Relative expression of PuAAT1 (A); PuCXE7 (B); PuCXE15 (C); PuCXE20 (D); PuCXE25 (E). The white lines represent untreated fruit as a control group (CK), the yellow lines represent MeJA treatment, and the green lines represent DIECA treatment. Asterisks represent the significant difference between MeJA or DIECA treatment and the CK. Statistical significance: * p < 0.05, ** p < 0.01.
Horticulturae 10 00329 g006
Table 1. The content of ester volatile compounds in the OTP of Nanguo pears after postharvest 100 µM MeJA and 100 mM DIECA treatment.
Table 1. The content of ester volatile compounds in the OTP of Nanguo pears after postharvest 100 µM MeJA and 100 mM DIECA treatment.
No.CAS No.CompoundsRetention Times (min)CK
(ng/g)
100 µM MeJA
(ng/g)
100 mM DIECA
(ng/g)
1000141-78-6ethyl acetate2.547649.71 ± 62.33782.43 ± 68.75-
2000539-82-2ethyl valerate3.474-172.06 ± 3.43-
3000105-54-4ethyl butanoate5.2111569.65 ± 67.63287.3 ± 206.56422.89 ± 8.67
4000123-86-4butyl acetate5.87232.36 ± 0.47--
5000106-70-7methyl hexanoate6.260-172.96 ± 1.24-
6000123-66-0ethyl hexanoate13.2792808.22 ± 75.892693.77 ± 33.471417.61 ± 13.68
7000142-92-7hexyl acetate15.602259.84 ± 5.151723.94 ± 25.5-
8000106-30-9ethyl heptanoate16.147-36.99 ± 0.48-
9001552-67-6ethyl hex-2-enoate16.46839.49 ± 161.08 ± 1.78-
10000112-06-1heptylacetat18.64819.28 ± 0.428.6 ± 1.11-
11000106-32-1ethyl caprylate23.192-150.15 ± 3.04-
12007367-82-0ethyl (E)-2-octenoate27.552-85.98 ± 1.14-
13013327-56-5ethyl 3-methylthiopropionate28.01494.27 ± 1.37249.62 ± 6.53-
14006378-65-0hexyl hexanoate28.68910.56 ± 0.6643.25 ± 2.01-
15000110-38-3ethyl caprate29.28625.3 ± 0.85--
16002305-25-1ethyl 3-hydroxyhexanoate30.33326.9 ± 0.51--
17003025-30-7ethyl(2E,4Z)-deca-2,4-dienoate33.978192.46 ± 2.83189.55 ± 0.8-
18100140-77-5pentanoic acid, 2,2,4-trimethyl-3-carboxyisopropyl, isobutyl ester34.874-702.36 ± 10.69-
19000626-11-9diethyl 1-malate36.793192.5 ± 3.95107.36 ± 0.45-
20000628-97-7ethyl palmitate44.72939.5 ± 1.07--
CAS No.: Chemical Abstracts Service registry number; CK: fruit without any treatment; MeJA: fruit treated by MeJA; DIECA: fruit treated by DIECA.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Qi, L.; Li, C.; Sun, J.; Liu, W.; Yang, Y.; Li, X.; Li, H.; Du, Y.; Mostafa, I.; Yin, Z. Jasmonate Promotes Ester Aroma Biosynthesis during Nanguo Pears Storage. Horticulturae 2024, 10, 329. https://0-doi-org.brum.beds.ac.uk/10.3390/horticulturae10040329

AMA Style

Qi L, Li C, Sun J, Liu W, Yang Y, Li X, Li H, Du Y, Mostafa I, Yin Z. Jasmonate Promotes Ester Aroma Biosynthesis during Nanguo Pears Storage. Horticulturae. 2024; 10(4):329. https://0-doi-org.brum.beds.ac.uk/10.3390/horticulturae10040329

Chicago/Turabian Style

Qi, Liyong, Chuhan Li, Jianan Sun, Weiting Liu, Yueming Yang, Xiaojing Li, Hongjian Li, Yuqi Du, Islam Mostafa, and Zepeng Yin. 2024. "Jasmonate Promotes Ester Aroma Biosynthesis during Nanguo Pears Storage" Horticulturae 10, no. 4: 329. https://0-doi-org.brum.beds.ac.uk/10.3390/horticulturae10040329

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop