Next Article in Journal
ASC Regulates Subcutaneous Adipose Tissue Lipogenesis and Lipolysis via p53/AMPKα Axis
Next Article in Special Issue
Nitric Oxide Acts as an Inhibitor of Postharvest Senescence in Horticultural Products
Previous Article in Journal
Genome-Wide Analysis of the SPL Gene Family and Expression Analysis during Flowering Induction in Prunus × yedoensis ‘Somei-yoshino’
Previous Article in Special Issue
The Role of Alternative Oxidase in the Interplay between Nitric Oxide, Reactive Oxygen Species, and Ethylene in Tobacco (Nicotiana tabacum L.) Plants Incubated under Normoxic and Hypoxic Conditions
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 23
Issue 17
10.3390/ijms231710046
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Role of Nitric Oxide in Postharvest Senescence of Fruits

by
Changxia Li
1,*,
Wenjin Yu
1 and
Weibiao Liao
2
1
College of Agriculture, Guangxi University, Nanning 530004, China
2
College of Horticulture, Gansu Agricultural University, Lanzhou 730070, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2022, 23(17), 10046; https://doi.org/10.3390/ijms231710046
Submission received: 19 August 2022 / Revised: 29 August 2022 / Accepted: 1 September 2022 / Published: 2 September 2022
(This article belongs to the Special Issue Nitric Oxide Signalling and Metabolism in Plants)
Browse Figures
Versions Notes

Abstract

:
Nitric oxide (NO) acts as a gaseous signalling molecule and is considered to be a key regulator in the postharvest storage of fruits. Postharvest senescence is one of the most serious threats affecting the usage and economic value of fruits. Most recent studies have found that exogenous NO application can effectively improve the quality and prolong the shelf life of fruit postharvest by inhibiting postharvest diseases and alleviating chilling injury. Understanding the roles of NO is essential to elucidating how NO activates the appropriate set of responses to postharvest senescence. Here, we concluded that exogenous NO treatment alleviated senescence in postharvest fruit and attributed this to the following factors: (1) ethylene biosynthesis, (2) the antioxidant system, (3) polyamine metabolism and γ-aminobutyric acid (GABA) shunting, (4) cell wall metabolism, (5) sugar metabolism, (6) energy metabolism, (7) the CRT/DRE-binding factor (CBF) pathway and (8) S-nitrosylation. Moreover, crosstalk between NO and hydrogen sulfide (H2S), hydrogen peroxide (H2O2), oxalic acid (OA), arginine (Arg), GATA or plant hormone abscisic acid (ABA), melatonin (MT), and methyl jasmonate (MeJA), along with the regulation of key genes, were found to be very important in responses to postharvest senescence. In this study, we focus on the recent knowledge concerning the alleviative effect of NO on postharvest senescence, covering ethylene biosynthesis, the antioxidant system and related gene and protein expression.

1. Introduction

Fruits are widely consumed all over the world due to their good taste and their being rich in nutrients, such as vitamins, sugar, organic acids, and so on [1]. However, during postharvest storage, fruits are highly perishable and prone to browning, which is accompanied by a loss of taste and nutrients, directly affecting their acceptance by consumers and resulting in economic losses to fresh fruit producers [2,3]. Therefore, how to prolong the shelf life and maintain the quality of postharvest fruits has long been a focus of intense research.
Postharvest fruit senescence is a complex process affected by endogenous and exogenous environmental factors. It is well known that temperature is an important exogenous element that regulates the senescence of postharvest fruits, and low-temperature treatment is usually used as a positive effector in postharvest fruit preservation [4]. In addition, ethylene is a crucial endogenous factor in climacteric fruits because it can promote the process of senescence in harvested fruits. Thus, ethylene, as a negative factor, is usually inhibited by some new techniques in fruit storage to achieve the goal of prolonged postharvest senescence [5]. Moreover, it has been found that various signalling molecules play active roles in delaying senescence and maintaining the quality of postharvest fruits as positive effectors, such as nitric oxide (NO), hydrogen sulfide (H2S), melatonin (MT), etc. [6,7,8].
Since the discovery of the biological role of NO in plants, it has been understood that it acts as a gaseous signalling molecule that participates in a series of plant physiological processes, ranging from seed germination to root development to seedling growth [9]. NO is involved in the mechanism of plant response to abiotic stress, such as drought stress, low-temperature stress, heat stress, high salinity, ozone stress and heavy metal stress [10]. In general, endogenous NO is produced mainly through oxidation and reduction pathways [11,12] (Figure 1). In the oxidation pathway, nitric oxide synthase (NOS) catalyzes the production of NO from L-arginine, and in the reduction pathway for NO production nitrites are catalyzed by nitrate reductase (NR). In addition, some abiotic conditions also stimulate the release of endogenous NO [13]. Some studies have briefly described the direct role of NO in plant senescence, including fruits and leaves, and stress induction [14,15,16].
In view of the increasing interest in studies of NO in fruits, this paper provides a critical review of the most recent work in the literature regarding various mechanisms associated with the postharvest senescence of fruits in which NO plays a role and the interaction of NO with signalling molecules. In addition, genes the expression of which is mediated by NO during the postharvest senescence process are also briefly summarized. Therefore, this review may provide new ideas for future researchers studying the regulatory role of NO in postharvest fruit senescence. Additionally, it was an objective of this study to describe in detail the regulatory mechanisms that are relevant to the postharvest preservation of fruits in which NO is involved and further accelerate research into the use of NO in delaying postharvest fruit senescence.

2. Effects of NO in Postharvest Fruits

2.1. Delaying Postharvest Senescence

Some fleshy fruits, such as peaches, tomatoes and mangoes, are well known to have relatively short storage lives due to high respiration rates and thus accelerated fruit ripening and softening, which can significantly reduce their commercial value and impede marketing and sales. However, an increasing number of studies have reported that NO could prolong the shelf life of fruit during storage, which may have a positive impact on the fruit market (Table 1). NO was found to be effective in inhibiting the surface browning of apple slices [17]. Pristijono et al. [18] investigated changes in apple slice infiltration using an NO donor diethylenetriamine-nitric oxide (DETANO) solution for 60 s and found that NO could effectively inhibit the development of surface browning and extend postharvest life. It was also reported that the softening of harvested wax apple fruit was retarded by NO [19]. During storage at 18 °C, a higher NO content could further regulate apple fruit ripening [20]. Infiltration of strawberries with DETANO solution resulted in a similar extension of shelf life to that achieved by direct fumigation with NO gas [21]. The application of NO solution S-nitrosoglutathione (GSNO) delayed the postharvest senescence of blueberries [22]. NO might enhance the resistance of tissues to decay in Chinese bayberries [23]. In kiwifruit, prolonged shelf life was regulated by NO [6]. A delay in the initiation of the senescence of kiwifruits treated with NO, which extended postharvest shelf life, was observed [24]. It was also found that sodium nitroprusside (SNP) can be used as a dipping treatment before low-temperature storage to extend the shelf life of mango fruit [25]. NO could delay the colour development, softening and ripening of mango fruits during cold storage [26]. SNP treatment could effectively decay the softening and yellowing of postharvest mango fruit [27]. Banana fruits treated with NO maintained higher firmness than the control [28]. NO application could also delay the ripening of banana slices [29]. SNP was effective in reducing pistachio browning and extending postharvest life [30]. NO could also markedly delay the occurrence of flesh browning in jujube fruits [31]. NO could be used as a fresh-keeping agent to reduce the pericarp browning of litchis before storage [32]. Cornelian cherry fruits treated with SNP displayed remarkably lower fruit browning rates during cold storage [33]. The storage life of guavas can be prolonged by postharvest immersion treatment with SNP [34]. NO has a beneficial effect on the delay of postharvest grapefruit senescence [35]. NO treatment also significantly improved the shelf life of harvested pointed gourds [36]. Fruit ripening of harvested persimmon was significantly delayed by NO [37]. Singh et al. [38] reported that NO fumigation was effective in reducing skin colour changes and retarding softening in Japanese plums. SNP treatment is an easy method for the application of NO to extend the shelf life of plums during cold storage [39]. NO treatment may delay the senescence of peach fruits under cold conditions [40]. The application of NO could be a potential method for treating harvested tomato fruits in order to delay ripening [41]. Similarly, exogenous NO treatment was found to be a potential method for extending the postharvest life of citrus fruit [42]. NO treatment could effectively delay the softening and ripening of papaya fruit [43]. NO treatment could also effectively retard the ripening of oranges during storage [44].

2.2. Improving Postharvest Quality

More and more research has focused on the application of exogenous NO to improve the quality of postharvest fruits in recent years. Peach fruits fumigated with NO exhibited changes in colour, soluble solid contents (SSCs), titratable acidity (TA) and SSC/TA ratios during cold storage [5]. Guava fruits under NO treatment exhibited the minimum loss of chlorophyll, SSC and acidity, and a slower increase in carotenoid pigments [34] (Table 1). NO could increase the contents of vitamin C, organic acids and total soluble solids (SSs) in grapefruits during cold storage, suggesting that NO may have potential applications in postharvest treatments to maintain fruit quality [35]. NO application effectively maintained chlorophyll and suppressed the yellow colour development undergone by pointed gourds [36]. Preharvest peach fruits treated with NO exhibited higher levels of vitamin C compared to the control [45]. NO treatment significantly retarded increase in TSS content and decrease in TA content in winter jujubes during storage [31]. NO fumigation was effective in restricting changes in fructose, glucose, sucrose, sorbitol and TA contents and in skin colour during storage at 0 °C [26,38]. NO-treated mangos maintained higher contents of SSC and TA through the delay of ripening [27]. Throughout litchi storage, NO treatment effectively delayed loss of total SS, TA and ascorbic acid (ASA) contents in fruits [32]. Retarded colour change of peel and higher TA and TSS contents of pulp were shown in the ripening process of NO-treated banana fruits [46]. SNP treatment retained higher levels of TA and ASA in postharvest apples [47]. NO could protect kiwifruits against oxidative damage by maintaining contents of vitamins C and E during cold storage [48]. Exogenous NO treatment could improve the ASA and TA contents and delay increase in total SS contents in citrus fruits during storage at 20 °C [42]. NO significantly maintained a lower total anthocyanin content and a higher total phenol content, and delayed increase in SS and decrease in vitamin C contents in Chinese winter jujubes [49]. NO had a significant impact on the soluble sugar contents of peach fruits in room-temperature storage [50]. NO increased SSC⁄TA ratios, decreased SS contents and increased the vitamin C and E contents of kiwifruits, indicating that NO is effective in maintaining fruit quality during 20 °C storage [24]. NO treatment was responsible for higher levels of TA, soluble proteins, ASA and reducing sugars and lower levels of SSC in Hami melons, and retarded their ripening during storage [44]. Higher sucrose contents in peach fruits were sustained by NO treatment under cold conditions [40]. NO applications also slowed increase in SSC contents and SSC/TA ratios and decreased loss of TA and ASA contents in oranges during cold storage [51].

2.3. Inhibiting Postharvest Diseases

NO treatment effectively controlled brown rot disease caused by Monilinia fructicola in peach fruits [52]. Zheng et al. [53] and Table 1 show that lesion sizes in tomato fruits with Botrytis cinerea were reduced by 93.3 and 80.9% three and four days after NO inoculation, respectively, suggesting that NO could mitigate disease symptoms during storage. Lai et al. [41] showed that expression levels of the fruit-ripening-related genes LeACS2, LeACS4, LeACO1, LePG, LePhy1 and LePM were regulated by NO treatment, resulting in an increase in the resistance of tomato fruits to gray mold rot caused by Botrytis cinerea. Lesion development on mango fruits inoculated with Colletotrichum gloeosporioides was effectively suppressed by NO treatment during storage. NO treatment also significantly reduced natural anthracnose incidence in ripened mango fruits at ambient temperature [27]. SNP could markedly suppress the mycelial growth and spore germination of Colletotrichum gloeosporioides, resulting in delayed senescence in postharvest mango fruits [14]. NO treatment was a promising approach to improve resistance against fungal pathogens and maintain the quality of custard apples after harvest [47]. The resistance of pitaya fruit against anthracnose was also effectively enhanced by NO [54]. Use of exogenous NO was a promising method for inducing the disease resistance of fruits to fungal pathogens and extend the postharvest life of citrus fruits [42]. Liu et al. [44] indicated that NO treatment could effectively reduce disease incidence in oranges inoculated with Collletotichum goeosporioides and inhibit the increase in lesion diameters during storage.

2.4. Alleviating Chilling Injury

Ghorbani et al. [35] reported that NO could reduce chilling injury (CI) to harvested peach fruits during storage. NO reduced the incidence of CI by 1.5- to 1.7-fold in mango fruits [25] (Table 1). CI symptoms were significantly lower in NO-fumigated fruit than in non-fumigated fruit [38]. NO treatment significantly reduced the CI indexes of mango fruits during cold storage [26]. NO successfully alleviated CI in orange fruits [55]. NO treatment improved the chilling tolerance of banana fruits, as shown by reduced CI indexes after cold storage [46]. Application of NO could effectively reduce chilling injury to banana fruits [56]. NO could significantly control CI and improve resistance against chilling stress [57]. In Chinese bayberries, fumigation with NO inhibited ethylene release and disease incidence during cold storage [23]. NO treatment could alleviate and delay CI in cold-stored Hami melon fruits [58].

3. The Regulatory Pathways Prolonged by NO during Fruit Storage

3.1. Ethylene Biosynthesis

It is widely known that ethylene plays a vital regulatory role in the senescence process of harvested fruits [1]. NO, as a signal molecule regulator, is thought to be closely associated with inhibition of ethylene production in events that prolong the shelf life of fruits [67] (Figure 2). In NO-treated tomato fruits, expression levels of the LeACO1, LeACOH2 and LeACO4 genes were decreased and delayed [59] (Table 1). Lai et al. [41] also showed that NO suppressed rates of ethylene production during tomato fruit storage. NO fumigation inhibited ethylene biosynthesis in mango fruits by restraining 1-aminocyclopropane-1-carboxylate synthase (ACS) and ACC oxidase (ACO) activities, leading to reduced ACC contents during cold storage [26]. Subsequently, to further verify the roles of NO in postharvest mango fruits, Barman et al. [25] found that with dipping in SNP the rate of ethylene production in mango fruits was decreased by 117–270% compared to the control fruit dipped in distilled water. In apples, SNP treatment could increase the NO contents of harvested fruits during storage, while higher NO contents could further regulate fruit senescence by regulating ethylene production during storage at 18 °C [20]. Tareen et al. [5] indicated that NO exhibited synergistic effects in the reduction of ethylene production during peach fruit cold storage. In pear storage, the expression levels of the PcACS and PcACO genes were inhibited by MT and NO treatment [60]. To sum up, the inhibition of ethylene by NO-mediated ACC/ACS activity is not directly brought about through signal regulation.

3.2. Antioxidant System

The softening and senescence of postharvest fruits are usually accompanied by the generation of reactive oxygen species (ROS) [68]. Antioxidants significantly combat the oxidation of a series of substrates [69] and protect different biomolecules from the effects of damaging ROS by reacting with free radicals and preventing oxidation processes. Fruits are known to be rich sources of natural antioxidants either in the form of enzymes, such as superoxide dismutase (SOD), catalase (CAT), peroxidase (POD) and polyphenol oxidase (PPO), or in the form of non-enzymes, such as vitamins, including alpha tocopherol, carotenoids and ASA [69]. NO acts as a highly reactive free radical gas that participates in the resistance of fruits to senescence. Pistachios treated with NO maintained higher SOD, PPO and POD activities, which led to delayed hull browning [30] (Figure 2). NO significantly reduced lipid peroxidation as well as malondialdehyde (MDA) and hydrogen peroxide (H2O2) contents in grapefruits during cold storage. Simultaneously, the activities of antioxidant enzymes, such as POD, APX, SOD and catalase (CAT), were also enhanced by NO during this process [35]. Jujubes treated with NO exhibited higher activities of CAT, SOD, GR and APX [31] (Table 1). Simultaneously, reductions in ASA and glutathione (GSH) contents and increases in superoxide anion (O2−) production and H2O2 contents were also delayed by NO treatment [31]. ROS accumulation and the lipid peroxidation of membranes were alleviated by NO through the induction of APX, SOD, POD, CAT and GR activities in the peel and pulp of table grapes [3]. NO successfully alleviated CI in orange fruits by inducing antioxidant responses, whilst maintaining fruit quality by decreasing H2O2 contents and lipid peroxidation [55]. The minimum loss of phenols, flavonoids, antioxidant capacity and radical scavenging activity were exhibited by guava fruits treated with NO [34]. Application of SNP retained greater total antioxidant activities and phenolic compound contents in harvested persimmon fruits [37]. During storage, contents of total flavonoids, phenolics, hydroxyproline-rich glycoproteins and lignin were elevated by NO in kiwifruit [6]. NO could also protect kiwifruits against oxidative damage caused by ROS during storage [48]. Contents of ASA and glutathione were improved by NO during the postharvest storage of blueberries [22]. Application of NO could effectively reduce CI in banana fruits by decreasing O2− production and H2O2 contents, increas activities of POD, SOD, CAT and APX, and up-regulating expression levels of the MaPOD, MaSOD, MaCAT and MaAPX genes [56]. Chinese bayberry fumigation with NO delayed the decrease in total phenolic contents and DPPH radical scavenging activities, while increases in both the rate of O2− production and H2O2 content were delayed, followed by increases in the activities of SOD, CAT and APX during storage [23]. Kiwifruits treated with NO had lower contents of soluble solids and MDA and higher contents of vitamins C and E during 20 °C storage [24]. Inhibition of the browning of peach slices by NO via the antioxidant system was discussed by Zhu et al. [62]. NO also effectively decreased the production of MDA, O2− and H2O2 in longkong fruits during storage [57]. Meanwhile, NO-treated longkong fruit pericarps exhibited lower activities of browning-related enzymes, including PAL and PPO, and higher activities of antioxidant enzymes, including POD, SOD, CAT and GPX, than the control, suggesting that NO could significantly prolong the shelf life of longkong fruit during cold storage [57]. Application of NO effectively suppressed lignin formation and electrolyte leakage and maintained contents of chlorophyll and phenolics as well as membrane integrity in pointed gourds during storage. The activities of PAL and LOX enzymes in pointed gourds were also influenced positively by NO application during this process [36]. NO was positively correlated with pericarp browning in litchis due to reduced MDA contents [32]. Wang et al. [46] showed that activities of POD, CAT and APX were increased by NO in banana fruits after cold storage. Additionally, the antioxidant activities of DPPH and FRAP were enhanced by NO in custard apples during storage [47].

3.3. Polyamine Metabolism and GABA Shunting

Polyamines (PAs) mainly include spermidine (Spd), putrescine (Put) and spermine (Spm), which are widely found in plant tissues. In the biosynthesis pathway of Pas, the decarboxylation of ornithine and arginine is catabolized by ornithine decarboxylase (ODC) and arginine decarboxylase (ADC), respectively, to produce Put [70] (Figure 2). Spd and Spm can be synthesized from Put by the sequential addition of aminopropyl groups [71]. Diamine oxidase (DAO) and polyamine oxidase (PAO) catalyze the degradation of polyamines [72,73]. Polyamine metabolism is closely associated with γ-aminobutyric acid (GABA) and proline. Briefly, Put can be converted into GABA, catalyzed by DAO [72,73,74] (Figure 2). In recent years, the regulatory roles of PAs and GABA shunting in postharvest fruit senescence have been well established [61] (Table 1). Wang et al. [61] indicated that NO-induced chilling tolerance might be ascribed to the enhanced catabolism of PAs, GABA and proline in banana fruits. Cherry fruits treated with NO and GABA exhibited significantly lower fruit browning rates during cold storage, which may be ascribed to lower MDA and H2O2 contents and LOX activity and higher CAT, SOD, APX and GR activities, suggesting that applications of NO and GABA may be promising strategies for delaying the postharvest senescence of fruits [33].

3.4. Cell Wall Metabolism

NO mediated the activities of cell-wall-softening-related enzymes, which could effectively inhibit the softening of papaya fruits [43]. SNP is a simple NO application method for inhibiting fruit softening, maintaining fruit quality and prolonging shelf life by interfering with PAL and PME activities in ‘Santa Rosa’ plums during cold storage [39] (Table 1). NO-mediated cell wall metabolism inhibited the browning of peach slices by increasing PAL activity [62]. NO increased the activity of cell-wall-metabolism-related enzymes, such as CoA ligase (4CL), phenylalanine ammonia-lyase (PAL), polyphenol oxidase (PPO), β-1,3-glucanase (GLU) and chitinase (CHI), which might be beneficial for the retardation of senescence in pitaya fruits during storage [54]. NO also increased the activities of PAL, POD and β-1,3-glucanase during kiwifruit storage [6].

3.5. Sugar Metabolism

Soluble sugars, such as fructose, glucose and sucrose, are considered to be signal molecules that participate in the senescence of harvested fruits. Shi et al. [63] (Table 1) found that red raspberries treated with NO showed increased sucrose synthase (SS), sucrose phosphate synthase (SPS) and neutral invertase (NI) activities; decreased acid invertase (AI) activity; and higher fructose, glucose and sucrose contents. It has been reported that NO improved the quality of apple fruits by increasing the activities of sucrose synthase synthesis (SS-s) and SPS and decreasing sucrose synthase cleavage (SS-c), NI and AI activities, following which the expression levels of the MdSPS, MdSS, MdNI, hexokinase (HK) and fructokinase (FK) genes were significantly up-regulated [64]. Similarly, NO sustained higher sucrose contents and lower glucose and fructose contents in peach fruits under cold conditions by enhancing SPS activity and the expression levels of the PpaSPS1/2 gene and decreasing SS-c activity by reducing expression levels of the PpaAI1 sucrose-cleaving enzyme gene [40].

3.6. Energy Metabolism

Sugar is important not only as a factor determining fruit quality but also as a substrate for energy supply. Maintaining adequate energy supply is essential for delaying the postharvest senescence of fruits. NO could extend the duration of cold storage time for banana fruits by increasing contents of energy charge and adenosine triphosphate (ATP) and the activities of Ca2+-ATPase, H+-ATPase, succinic dehydrogenase (SDH) and cytochrome C oxidase (CCO) enzymes [46] (Table 1).

3.7. CBF Pathway

It is reported that CRT/DRE-binding factors (CBFs), as transcription factors, improve the chilling tolerance of fruits, while expression of the cold response gene (COR) gene is activated by recognition and binding of the C-repeat/dehydration-responsive element (CRT/DRE) cis-element [75]. Zhao et al. [65] showed that treatment of tomatoes with SNP resulted in up-regulation of the expression of stress response genes via enhanced expression of the LeCBF1 gene, which thereby enhanced tolerance to cold stress during storage. Hami melon fruits fumigated with NO gas showed up-regulated expression levels of the CmCBF1 and CmCBF3 genes, which led to the alleviation of chilling injury during cold storage [58] (Table 1).

3.8. S-Nitrosylation

Protein S-nitrosylation, as a key post-translational modification, has been reported in the processes of fruit storage, salt stress and so on [66,76]. NO inhibited the gene expression, S-nitrosylation and activity of GSNOR, demonstrating that S-nitrosylation of GSNOR proteins was effective in prolonging the storage life of peach fruits and preserving them against disease; in addition, NO and GSNOR inhibitors up-regulated the relative expression of systemic acquired resistance (SAR)-related genes, including the non-expressor of PR1 (NPR1), pathogenesis-related gene 1 (PR1) and TGACG-binding factor 1 (TGA1) [66] (Table 1). Studies on the way in which NO-mediated S-nitrosylation modulates postharvest fruit senescence are quite limited. Therefore, it will be necessary for future studies to examine the NO-mediated S-nitrosylation of specific proteins and specific S-nitrosylation sites in this process.

4. Potential Networks of Crosstalk Involving NO and Other Signalling Molecules in the Regulation of Postharvest Fruit Senescence

Previous studies have shown that NO can interact with other molecules to extend the shelf lives of preharvest fruits, suggesting that NO signal transduction is not generally a linear pathway. Here, we provide a brief overview of the interactions between NO and H2S, H2O2, plant hormones and other signalling molecules during storage (Figure 3).
Peach fruits fumigated with NO combined with the ethylene inhibitor aminoethoxyvinylglycine (AVG) exhibited longer storage lives compared to those that received NO treatment alone [5] (Figure 3A). Wu et al. [23] showed that combined treatment with 1-methylcyclopropene (1-MCP) and NO had a functional synergistic effect in peach fruits. Ethylene-related genes, including MiACS, MiACO, MiETR1, MiEIN2, MiERS1 and MiERF, might be involved in the NO and SA signal induction pathways during storage [77] (Figure 3A). Steelheart et al. [78] demonstrated that NO improved the effect of 1-MCP on the extension of the storage life of postharvest tomatoes (Figure 3A). Zhu et al. [79] also indicated that combinatorial treatment (NO+H2S) maintained a superior quality of peach fruits by inhibiting ethylene synthesis and cell wall metabolism (Figure 3B). NO-mediated H2S metabolism regulated the postharvest senescence of peach fruits by reducing endogenous H2S, sulfite and Cys contents; decreasing the activities of O-acetylserine (thiol)lyase (OAS-TL), l-/d-cysteine desulfhydrase (l-/d-CD) and sulfite reductase (SiR); and increasing β-cyanoalanine synthase (β-CAS) activity [80] (Figure 3B). H2O2 was required for NO-mediated disease resistance in harvested tomato fruits during storage [81] (Figure 3B). Mohamed et al. [51] reported that postharvest treatments of 1 mM SNP combined with 10 mM oxalic acid (OA) or 2% H2O2 are good potential strategies for delaying senescence as well as maintaining the quality of oranges during cold storage (Figure 3B). Arg-mediated NOS pathway activity improved the quality and delayed the postharvest senescence of strawberry fruits [82] (Figure 3C). Exogenous NO enhanced the chilling resistance of harvested peach fruits by inducing SA or JA signalling [54] (Figure 3C). MeJA may function upstream of and depend on NO in the signalling pathway that activates chilling tolerance in cucumber during storage [83] (Figure 3C). Exogenous ABA application could enhance lily bulb resistance to cold-induced oxidative stress by improving the efficiency of enzymatic and non-enzymatic systems which were found to be partially mediated by NO [4] (Figure 3C). MT acted as an upstream signal of NO synthesis and delayed postharvest senescence in pear fruits [60] (Figure 3C).

5. Modulation of Gene Expression by NO during Fruit Storage

As mentioned above, a series of potential mechanisms involving NO have been confirmed in the delayed senescence of postharvest fruits. Thus, some genes must inevitably be changed following exposure to NO (Table 2). For example, NO induced VvSOD, VvCAT, VvPOD2 and VvGR expression [3]. Banana fruits treated with NO exhibited higher expression levels of MaSOD, MaCAT, MaPOD and MaAPX than the control during storage [56]. NO could delay kiwifruit senescence during storage, in which relative expression of the POD, PAL and CHT genes was up-regulated [6]. The expression of SsC4H was down-regulated in the NO-retarded cottony softening of harvested wax apple fruits [19]. NO also up-regulated relative expression of the LeACO1, LeACOH2 and LeACO4 genes during tomato storage [71]. The expression levels of LeACS2, LeACS4, LeACO1, LePG, LePhy1 and LePME were regulated by NO during cold storage [41]. MT plus NO treatment inhibited the expression levels of the PcACS and PcACO genes, decreased the rate of up-regulation of PcCel and PcPG, and up-regulated the relative expression of PcNOS, implying that MT, as an upstream signalling molecule of NO, delayed senescence in pear fruits [60]. Additionally, NO treatment protected tomatoes from cold injury by inducing expression of the LeCBF1 gene [65]. NO also could prolong the storage life of Hami melon fruits by up-regulating the expression levels of the CmCBF1 and CmCBF3 genes [58]. NO improved the quality of apple fruits by up-regulating the relative expression of the MdSS, MdSPS, MdNI, FK and HK genes [64]. Similarly, NO maintained the high quality of peach fruits during cold storage by up-regulating the SPS-related gene PpaSPS1/2 and down-regulating the SS-c-related gene PpaAI1 [40]. Moreover, NO inhibited gene expression of GSNOR and up-regulated expression of SAR-related genes, including NPR1, PR1 and TGA1, suggesting that S-nitrosylation of GSNOR contributed to improved shelf life in peach fruits [66].

6. Conclusions and Future Perspective

In conclusion, in fruits, NO could delay postharvest senescence and maintain postharvest quality by inhibiting postharvest diseases and alleviating chilling injury. The regulation of ethylene biosynthesis, the antioxidant system, polyamine metabolism, GABA shunting, cell wall metabolism, sugar metabolism, energy metabolism, the CBF pathway and S-nitrosylation by NO are essential strategies for prolonging the storage life of fruits. Additionally, we have also reviewed the crosstalk mechanisms that are associated with applications of exogenous NO, H2S, H2O2, OA, Arg, GATA, plant hormone ABA, MT and MeJA in postharvest fruit preservation. Moreover, NO can regulate the expression of responsive genes during this process. These insights might help guide future postharvest fruit preservation strategy design, ultimately leading to effective preservatives better suited to our agricultural requirements.
Future studies regarding the regulatory role of NO in postharvest senescence should focus on the molecular details of the particular pathways that are activated in fruits. Nowadays, although it is a well-known fact that NO interacts with other gas signalling molecules or phytohormones in response to the postharvest senescence of fruits, the signal transduction pathway involved in this crosstalk mechanism still needs to be further elucidated. Clearly, S-nitrosylated proteins are quite limited during postharvest senescence. Future work is needed to detect more S-nitrosylated candidates in postharvest fruit senescence in order to understand the complicated functions of S-nitrosylation during this process. More research work will improve knowledge concerning possible applications of NO solutions to postharvest horticultural products with the aim of enhancing their quality and economic value.

Author Contributions

Conceptualization, C.L.; methodology, C.L., W.Y. and W.L.; formal analysis, C.L., W.Y. and W.L.; writing—original draft preparation, C.L.; writing—review and editing, C.L. and W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Nature Science Foundation of China (31660568), Guangxi science and technology major project (GuikeAA22068088) and start-up funding for introduced talents in Guangxi University (to C.L.).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Zhang, W.; Jiang, W. UV treatment improved the quality of postharvest fruits and vegetables by inducing resistance. Trends. Food Sci. Technol. 2019, 92, 71–80. [Google Scholar] [CrossRef]
  2. Kerch, G. Chitosan films and coatings prevent losses of fresh fruit nutritional quality: A review. Trends. Food Sci. Technol. 2015, 46, 159–166. [Google Scholar] [CrossRef]
  3. Zhang, Z.; Xu, J.; Chen, Y.; Wei, J.; Wu, B. Nitric oxide treatment maintains postharvest quality of table grapes by mitigation of oxidative damage. Postharvest Biol. Technol. 2019, 152, 9–18. [Google Scholar] [CrossRef]
  4. Zhang, D.N.; Guo, X.Y.; Chen, Z.G. A novel and efficient method for the isolation and purification of polysaccharides from lily bulbs by Saccharomyces cerevisiae fermentation. Process Biochem. 2014, 49, 2299–2304. [Google Scholar] [CrossRef]
  5. Tareen, M.J.; Singh, Z.; Khan, A.S.; Abbasi, N.A.; Naveed, M. Combined applications of aminoethoxyvinylglycine with salicylic acid or nitric oxide reduce oxidative stress in peach during ripening and cold storage. J. Plant Growth Regul. 2017, 36, 983–994. [Google Scholar] [CrossRef]
  6. Zheng, X.L.; Hu, B.; Song, L.J.; Pan, J.; Liu, M.M. Changes in quality and defense resistance of kiwifruit in response to nitric oxide treatment during storage at room temperature. Sci. Hortic. 2017, 222, 187–192. [Google Scholar] [CrossRef]
  7. Ali, S.; Nawaz, A.; Ejaz, S.; Haider, S.T.A.; Alam, M.W.; Javed, H.U. Effects of hydrogen sulfide on postharvest physiology of fruits and vegetables: An overview. Sci. Hortic. 2019, 243, 290–299. [Google Scholar] [CrossRef]
  8. Aghdam, M.S.; Luo, Z.; Li, L.; Jannatizadeh, A.; Fard, J.R.; Pirzad, F. Melatonin treatment maintains nutraceutical properties of pomegranate fruits during cold storage. Food Chem. 2020, 303, 125385. [Google Scholar] [CrossRef]
  9. Corpas, F.; Palma, J. Assessing nitric oxide (NO) in higher plants: An outline. Nitrogen 2020, 1, 12–20. [Google Scholar] [CrossRef]
  10. Fancy, N.N.; Bahlmann, A.K.; Loake, G.J. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 2017, 40, 462–472. [Google Scholar] [CrossRef] [Green Version]
  11. Guo, F.Q.; Okamoto, M.; Crawford, N.M. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 2003, 302, 100–103. [Google Scholar] [CrossRef]
  12. Jasid, S.; Simontacchi, M.; Bartoli, C.G.; Puntarulo, S. Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol. 2006, 142, 1246–1255. [Google Scholar] [CrossRef] [PubMed]
  13. Wei, L.J.; Zhang, J.; Wang, C.L.; Liao, W.B. Recent progress in the knowledge on the alleviating effect of nitric oxide on heavy metal stress in plants. Plant Physiol. Biochem. 2020, 147, 161–171. [Google Scholar] [CrossRef] [PubMed]
  14. Ren, Y.; Xue, Y.; Tian, D.; Zhang, L.; Xiao, G.; He, J. Improvement of postharvest anthracnose resistance in mango fruit by nitric oxide and the possible mechanisms involved. J. Agric. Food Chem. 2020, 68, 15460–15467. [Google Scholar] [CrossRef] [PubMed]
  15. Du, J.; Li, M.L.; Kong, D.D.; Wang, L.; Lv, Q.; Wang, J.Z.; Bao, F.; Gong, Q.Q.; Xia, J.C.; He, Y.K. Nitric oxide induces cotyledon senescence involving co-operation of the NES1/MAD1 and EIN2-associated ORE1 signalling pathways in Arabidopsis. J. Exp. Bot. 2013, 65, 4051–4063. [Google Scholar] [CrossRef] [PubMed]
  16. Terrón-Camero, L.C.; Peláez-Vico, M.Á.; Del-Val, C.; Sandalio, L.M.; Romero-Puertas, M.C. Role of nitric oxide in plant responses to heavy metal stress: Exogenous application versus endogenous production. J. Exp. Bot. 2019, 70, 4477–4488. [Google Scholar] [CrossRef]
  17. Pristijono, P.; Wills, R.B.H.; Golding, J.B. Inhibition of browning on the surface of apple slices by short term exposure to nitric oxide (NO) gas. Postharvest Biol. Technol. 2006, 42, 256–259. [Google Scholar] [CrossRef]
  18. Pristijono, P.; Wills, R.B.H.; Golding, J.B. Use of the nitric oxide-donor compound, diethylenetriamine-nitric oxide (DETANO), as an inhibitor of browning in apple slices. J. Hortic. Sci. Biotechnol. 2008, 83, 555–558. [Google Scholar] [CrossRef]
  19. Huang, L.N.; Wu, G.B.; Zhang, S.; Kuang, F.Y.; Chen, F.H. The identification and functional verification of the cinnamate 4-hydroxylase gene from wax apple fruit and its role in lignin biosynthesis during nitric oxide-delayed postharvest cottony softening. Postharvest Biol. Technol. 2019, 158, 110964. [Google Scholar] [CrossRef]
  20. Deng, L.; Pan, X.; Chen, L.; Shen, L.; Sheng, J. Effects of preharvest nitric oxide treatment on ethylene biosynthesis and soluble sugars metabolism in ‘Golden Delicious’ apples. Postharvest Biol. Technol. 2013, 84, 9–15. [Google Scholar] [CrossRef]
  21. Wills, R.B.H.; Soegiarto, L.; Bowyer, M.C. Use of a solid mixture containing diethylenetriamine/nitric oxide (DETANO) to liberate nitric oxide gas in the presence of horticultural produce to extend postharvest life. Nitric Oxide 2007, 17, 44–49. [Google Scholar] [CrossRef] [PubMed]
  22. Grozeff, G.E.G.; Alegre, M.L.; Senn, M.E.; Chaves, A.R.; Simontacchi, M.; Bartoli, C.G. Combination of nitric oxide and 1-MCP on postharvest life of the blueberry (Vaccinium spp.) fruit. Postharvest Biol. Technol. 2017, 133, 72–80. [Google Scholar] [CrossRef]
  23. Wu, F.H.; Yang, H.Q.; Chang, Y.Z.; Cheng, J.Y.; Bai, X.S.F.; Yin, J.Y. Effects of nitric oxide on reactive oxygen species and antioxidant capacity in Chinese Bayberry during storage. Sci. Hortic. 2012, 135, 106–111. [Google Scholar] [CrossRef]
  24. Zhu, S.H.; Sun, L.N.; Zhou, J. Effects of different nitric oxide application on quality of kiwifruit during 20 °C storage. Int. J. Food Sci. Technol. 2010, 45, 245–251. [Google Scholar] [CrossRef]
  25. Barman, K.; Asrey, R.; Pal, R.K.; Jha, S.K.; Bhatia, K. Post-harvest nitric oxide treatment reduces chilling injury and enhances the shelf-life of mango (Mangifera indica L.) fruit during low-temperature storage. J. Horticul. Sci. Biotechnol. 2014, 89, 253–260. [Google Scholar] [CrossRef]
  26. Zaharah, S.S.; Singh, Z. Postharvest nitric oxide fumigation alleviates chilling injury, delays fruit ripening and maintains quality in cold-stored ‘Kensington Pride’ mango. Postharvest Biol. Technol. 2011, 60, 202–210. [Google Scholar] [CrossRef]
  27. Hu, M.; Yang, D.; Huber, D.J.; Jiang, Y.; Li, M.; Gao, Z.; Zhang, Z. Reduction of postharvest anthracnose and enhancement of disease resistance in ripening mango fruit by nitric oxide treatment. Postharvest Biol. Technol. 2014, 97, 115–122. [Google Scholar] [CrossRef]
  28. Wang, Y.S.; Luo, Z.S.; Du, R.X.; Liu, Y.; Ying, T.J.; Mao, L.C. Effect of nitric oxide on antioxidative response and proline metabolism in banana during cold storage. J. Agric. Food Chem. 2013, 61, 8880–8887. [Google Scholar] [CrossRef]
  29. Cheng, G.P.; Yang, E.; Lu, W.J.; Jia, Y.X.; Jiang, Y.M.; Duan, X.W. Effect of nitric oxide on ethylene synthesis and softening of banana fruit slice during ripening. J. Agric. Food Chem. 2009, 57, 5799–5804. [Google Scholar] [CrossRef]
  30. Gheysarbigi, S.; Mirdehghan, S.H.; Ghasemnezhad, M.; Nazoori, F. The inhibitory effect of nitric oxide on enzymatic browning reactions of in-package fresh pistachios (Pistacia vera L.). Postharvest Biol. Technol. 2020, 159, 110998. [Google Scholar] [CrossRef]
  31. Zhao, Y.T.; Zhu, X.; Hou, Y.Y.; Wang, X.Y.; Li, X.H. Postharvest nitric oxide treatment delays the senescence of winter jujube (Zizyphus jujuba mill. cv. Dongzao) fruit during cold storage by regulating reactive oxygen species metabolism. Sci. Hortic. 2020, 261, 109009. [Google Scholar] [CrossRef]
  32. Barman, K.; Siddiqui, M.W.; Patel, V.B.; Prasad, M. Nitric oxide reduces pericarp browning and preserves bioactive antioxidants in litchi. Sci. Hortic. 2014, 171, 71–77. [Google Scholar] [CrossRef]
  33. Rabiei, V.; Kakavand, F.; Zaare-Nahandi, F.; Razavi, F.; Aghdam, M.S. Nitric oxide and γ-aminobutyric acid treatments delay senescence of cornelian cherry fruits during postharvest cold storage by enhancing antioxidant system activity. Sci. Hortic. 2019, 243, 268–273. [Google Scholar] [CrossRef]
  34. Sahu, S.K.; Barman, K.; Singh, A.K. Nitric oxide application for postharvest quality retention of guava fruits. Acta Physiol. Plant 2020, 42, 156. [Google Scholar] [CrossRef]
  35. Ghorbani, B.; Pakkish, Z.; Najafzadeh, R. Shelf life improvement of grape (Vitis vinifera L. cv. Rish Baba) using nitric oxide (NO) during chilling damage. Int. J. Food Prop. 2017, 20, 2750–2763. [Google Scholar] [CrossRef]
  36. Siddiqui, M.W.; Homa, F.; Lata, D.; Ahmag, M.S. Exogenous nitric oxide delays ripening and maintains postharvest quality of pointed gourd during storage. J. Plant Growth Regul. 2021, 40, 2371–2378. [Google Scholar] [CrossRef]
  37. Shahkoomahally, S.; Ramezanian, A.; Farahnaky, A. Postharvest nitric oxide treatment of persimmon (Diospyros kaki L.) improves fruit quality during storage. Fruits 2015, 70, 63–68. [Google Scholar] [CrossRef]
  38. Singh, S.P.; Singh, Z.; Swinny, E.E. Postharvest nitric oxide fumigation delays fruit ripening and alleviates chilling injury during cold storage of Japanese plums (Prunus salicina Lindell). Postharvest Biol. Technol. 2009, 53, 101–108. [Google Scholar] [CrossRef]
  39. Sharma, S.; Sharma, R.R. Nitric oxide inhibits activities of PAL and PME enzymes and reduces chilling injury in ‘Santa Rosa’ Japanese plum (Prunus salicina Lindell). J. Plant Biochem. Biot. 2015, 24, 292–297. [Google Scholar] [CrossRef]
  40. Han, S.; Cai, H.; An, X.; Huan, C.; Wu, X.; Jiang, L.; Yu, Z. Effect of nitric oxide on sugar metabolism in peach fruit (cv. Xiahui 6) during cold storage. Postharvest Biol. Technol. 2018, 142, 72–80. [Google Scholar] [CrossRef]
  41. Lai, T.; Wang, Y.; Li, B.; Qin, G.; Tian, S. Defense responses of tomato fruit to exogenous nitric oxide during postharvest storage. Postharvest Biol. Technol. 2011, 62, 127–132. [Google Scholar] [CrossRef]
  42. Zhou, Y.H.; Li, S.M.; Zeng, K.F. Exogenous nitric oxide-induced postharvest disease resistance in citrus fruit to Colletotrichum gloeosporioides. J. Sci. Food Agric. 2016, 81, 58–76. [Google Scholar] [CrossRef] [PubMed]
  43. Guo, Q.; Wu, B.; Chen, W.; Zhang, Y.; Wang, J.; Li, X. Effects of nitric oxide treatment on the cell wall softening related enzymes and several hormones of papaya fruit during storage. Food Sci. Technol. Int. 2014, 20, 309–317. [Google Scholar] [CrossRef] [PubMed]
  44. Liu, L.D.; Wang, J.J.; Qu, L.W.; Li, S.M.; Wu, R.Z.; Zeng, K.F. Effect of nitric oxide treatment on storage quality of glorious oranges. Procedia Eng. 2012, 37, 150–154. [Google Scholar] [CrossRef]
  45. Saba, M.K.; Moradi, S. Sodium nitroprusside (SNP) spray to maintain fruit quality and alleviate postharvest chilling injury of peach fruit. Sci. Hortic. 2017, 216, 193–199. [Google Scholar] [CrossRef]
  46. Wang, Y.S.; Luo, Z.S.; Khan, Z.U.; Mao, L.C.; Ying, T.J. Effect of nitric oxide on energy metabolism in postharvest banana fruit in response to chilling stress. Postharvest Biol. Technol. 2015, 108, 21–27. [Google Scholar] [CrossRef]
  47. Khaliq, G.; Ullah, M.; Memon, S.A.; Ali, A.; Rashid, M. Exogenous nitric oxide reduces postharvest anthracnose disease and maintains quality of custard apple (Annona squamosa L.) fruit during ripening. J. Food Meas. Charact. 2021, 15, 707–716. [Google Scholar] [CrossRef]
  48. Zhu, S.H.; Sun, L.N.; Liu, M.M.; Zhou, J. Effect of nitric oxide on reactive oxygen species and antioxidant enzymes in kiwifruit during storage. J. Sci. Food Agric. 2008, 88, 2324–2331. [Google Scholar] [CrossRef]
  49. Zhu, S.H.; Sun, L.N.; Zhou, J. Effects of nitric oxide fumigation on phenolic metabolism of postharvest chinese winter jujube (Zizyphus jujuba Mill. cv. Dongzao) in relation to fruit quality. LWT-Food Sci. Technol. 2009, 42, 1009–1014. [Google Scholar] [CrossRef]
  50. Sun, Z.; Li, Y.; Zhou, J.; Zhu, S.H. Effects of exogenous nitric oxide on contents of soluble sugars and related enzyme activities in ‘Feicheng’ peach fruit. J. Sci. Food Agric. 2011, 91, 1795–1800. [Google Scholar] [CrossRef]
  51. Mohamed, M.A.A.; Abd El-khalek, A.F.; Elmehrat, H.G.; Mahmoud, G.A. Nitric oxide, oxalic acid and hydrogen peroxide treatments to reduce decay and maintain postharvest quality of ‘Valencia’ orange fruits during cold storage. Egypt. J. Hortic. 2016, 43, 137–161. [Google Scholar]
  52. Shi, J.Y.; Liu, N.; Gu, R.X.; Zhu, L.Q.; Zhang, C.; Wang, Q.G.; Lei, Z.H.; Liu, Y.Y.; Ren, J.Y. Signals induced by exogenous nitric oxide and their role in controlling brown rot disease caused by monilinia fructicola in postharvest peach fruit. J. Gen. Plant Pathol. 2015, 81, 68–76. [Google Scholar] [CrossRef]
  53. Zheng, Y.; Shen, L.; Yu, M.M.; Fan, B.; Zhao, D.Y.; Liu, L.Y.; Sheng, J.P. Nitric oxide synthase as a postharvest response in pathogen resistance of tomato fruit. Postharvest. Biol. Technol. 2011, 60, 38–46. [Google Scholar] [CrossRef]
  54. Hu, M.; Zhu, Y.; Liu, G.; Gao, Z.; Li, M.; Su, Z.; Zhang, Z. Inhibition on anthracnose and induction of defense response by nitric oxide in pitaya fruit. Sci. Hortic. 2019, 245, 224–230. [Google Scholar] [CrossRef]
  55. Ghorbani, B.; Pakkish, Z.; Khezri, M. Nitric oxide increases antioxidant enzyme activity and reduces chilling injury in orange fruit during storage. N. Z. J. Crop Hortic. Sci. 2018, 46, 101–116. [Google Scholar] [CrossRef]
  56. Wu, B.; Guo, Q.; Li, Q.P.; Ha, Y.M.; Li, X.P.; Chen, W.X. Impact of postharvest nitric oxide treatment on antioxidant enzymes and related genes in banana fruit in response to chilling tolerance. Postharvest Biol. Technol. 2014, 92, 157–163. [Google Scholar] [CrossRef]
  57. Venkatachalam, K. Exogenous nitric oxide treatment impacts antioxidant response and alleviates chilling injuries in longkong pericarp. Sci. Hortic. 2018, 237, 311–317. [Google Scholar] [CrossRef]
  58. Zhang, T.; Che, F.B.; Zhang, H.; Pan, Y.; Xu, M.Q.; Ban, Q.Y.; Han, Y.; Rao, J.P. Effect of nitric oxide treatment on chilling injury, antioxidant enzymes and expression of the CmCBF1 and CmCBF3 genes in cold-stored Hami melon (Cucumis melo L.) fruit. Postharvest Biol. Technol. 2017, 127, 88–98. [Google Scholar] [CrossRef]
  59. Eum, H.L.; Kim, H.B.; Choi, S.B.; Lee, S.K. Regulation of ethylene biosynthesis by nitric oxide in tomato (Solanum lycopersicum L.) fruit harvested at different ripening stages. Eur. Food Res. Technol. 2009, 228, 331–338. [Google Scholar] [CrossRef]
  60. Liu, J.; Yang, J.; Zhang, H.; Cong, L.; Zhai, R.; Yang, C.; Xu, L. Melatonin inhibits ethylene synthesis via nitric oxide regulation to delay postharvest senescence in pears. J. Agric. Food Chem. 2019, 67, 2279–2288. [Google Scholar] [CrossRef]
  61. Wang, Y.S.; Luo, Z.S.; Mao, L.C.; Ying, T.J. Contribution of polyamines metabolism and GABA shunt to chilling tolerance induced by nitric oxide in cold-stored banana fruit. Food Chem. 2016, 197, 333–339. [Google Scholar] [CrossRef]
  62. Zhu, L.Q.; Zhou, J.; Zhu, S.H.; Guo, L.H. Inhibition of browning on the surface of peach slices by short-term exposure to nitric oxide and ascorbic acid. Food Chem. 2009, 114, 174–179. [Google Scholar]
  63. Shi, K.; Liu, Z.; Wang, J.; Zhu, S.; Huang, D. Nitric oxide modulates sugar metabolism and maintains the quality of red raspberry during storage. Sci. Hortic. 2019, 256, 108611. [Google Scholar] [CrossRef]
  64. Chen, Y.R.; Ge, Y.H.; Zhao, J.R.; Wei, M.L.; Li, C.Y.; Hou, J.B.; Cheng, Y.; Chen, J.G. Postharvest sodium nitroprusside treatment maintains storage quality of apple fruit by regulating sucrose metabolism. Postharvest Biol. Technol. 2019, 154, 115–120. [Google Scholar] [CrossRef]
  65. Zhao, R.R.; Sheng, J.P.; Lv, S.; Zheng, Y.; Zhang, J.; Yu, M.M.; Shen, L. Nitric oxide participates in the regulation of LeCBF1 gene expression and improves cold tolerance in harvested tomato fruit. Postharvest Biol. Technol. 2011, 62, 121–126. [Google Scholar] [CrossRef]
  66. Yu, Z.F.; Cao, J.; Zhu, S.H.; Zhang, L.L.; Peng, Y.; Shi, J.Y. Exogenous nitric oxide enhances disease resistance by nitrosylation and inhibition of s-nitrosoglutathione reductase in peach fruit. Front. Plant Sci. 2020, 11, 543. [Google Scholar] [CrossRef] [PubMed]
  67. Mukherjee, S. Recent advancements in the mechanism of nitric oxide signaling associated with hydrogen sulfide and melatonin crosstalk during ethylene-induced fruit ripening in plants. Nitric Oxide 2010, 82, 25–34. [Google Scholar] [CrossRef]
  68. Jing, G.; Zhou, J.; Zhu, S. Effects of nitric oxide on mitochondrial oxidative defence in postharvest peach fruits. J. Sci. Food Agric. 2016, 96, 1997–2003. [Google Scholar] [CrossRef] [PubMed]
  69. Halliwell, B. Antioxidant defence mechanisms: From the beginning to the end (of the beginning). Free Radic. Res. 1999, 31, 261–272. [Google Scholar] [CrossRef]
  70. Hussain, S.S.; Ali, M.; Ahmad, M.; Siddique, K.H.M. Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol. Adv. 2011, 29, 300–311. [Google Scholar] [CrossRef]
  71. Alcazar, R.; Altabella, T.; Marco, F.; Bortolotti, C.; Reymond, M.; Koncz, C.; Carrasco, P.; Tiburcio, A.F. Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta 2010, 231, 1237–1249. [Google Scholar] [CrossRef]
  72. Gupta, K.; Dey, A.; Gupta, B. Plant polyamines in abiotic stress responses. Acta Physiol. Plant. 2013, 35, 2015–2036. [Google Scholar] [CrossRef]
  73. Shelp, B.J.; Bozzo, G.G.; Trobacher, C.P.; Zarei, A.; Deyman, K.L.; Brikis, C.J. Hypothesis/review: Contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant. Sci. 2012, 193, 130–135. [Google Scholar] [CrossRef] [PubMed]
  74. Yang, R.Q.; Chen, H.; Gu, Z.X. Factors influencing diamine oxidase activity and gamma-aminobutyric acid content of fava bean (Vicia faba L.) during germination. J. Agric. Food Chem. 2011, 59, 11616–11620. [Google Scholar] [CrossRef] [PubMed]
  75. Aghdam, M.S.; Bodbodak, S. Physiological and biochemical mechanisms regulating chilling tolerance in fruits and vegetables under postharvest salicylates and jasmonates treatments. Sci. Hortic. 2013, 156, 73–85. [Google Scholar] [CrossRef]
  76. Wang, C.L.; Wei, L.J.; Zhang, J.; Hu, D.L.; Gao, R.; Liu, Y.Y.; Feng, L.; Gong, W.T.; Liao, W.B. Nitric oxide enhances salt tolerance in tomato seedlings by regulating endogenous S-nitrosylation levels. J. Plant Growth Regul. 2022, 1, 1–19. [Google Scholar] [CrossRef]
  77. Hong, K.; Gong, D.; Xu, H.; Wang, S.; Jia, Z.; Chen, J.; Zhang, L. Effects of salicylic acid and nitric oxide pretreatment on the expression of genes involved in the ethylene signalling pathway and the quality of postharvest mango fruit. N. Z. J. Crop Hortic. Sci. 2014, 42, 205–216. [Google Scholar] [CrossRef]
  78. Steelheart, C.; Alegre, M.L.; Bahima, J.V.; Senn, M.E.; Simontacchi, M.; Bartoli, C.G.; Esteban, G.; Grozeff, G. Nitric oxide improves the effect of 1-methylcyclopropene extending the tomato (Lycopersicum esculentum L.) fruit postharvest life. Sci. Hortic. 2019, 255, 193–201. [Google Scholar] [CrossRef]
  79. Zhu, L.Q.; Du, H.Y.; Wang, W.; Zhang, W.; Shen, Y.G.; Wan, C.P.; Chen, J.Y. Synergistic effect of nitric oxide with hydrogen sulfide on inhibition of ripening and softening of peach fruits during storage. Sci. Hortic. 2019, 256, 108591. [Google Scholar] [CrossRef]
  80. Geng, B.; Huang, D.; Zhu, S. Regulation of hydrogen sulfide metabolism by nitric oxide inhibitors and the quality of peaches during cold storage. Antioxidants 2019, 8, 401. [Google Scholar] [CrossRef]
  81. Fan, B.; Shen, L.; Liu, K.L.; Zhao, D.Y.; Yu, M.M.; Sheng, J.P. Interaction between nitric oxide and hydrogen peroxide in postharvest tomato resistance response to Rhizopus nigricans. J. Sci. Food Agric. 2008, 88, 1238–1244. [Google Scholar] [CrossRef]
  82. Shu, P.; Min, D.D.; Ai, W.; Li, J.Z.; Zhou, J.X.; Li, Z.L.; Zhang, X.H.; Shi, Z.D.; Sun, Y.J.; Jiang, Y.P.; et al. L-arginine treatment attenuates postharvest decay and maintains quality of strawberry fruit by promoting nitric oxide synthase pathway. Postharvest Biol. Technol. 2020, 168, 111253. [Google Scholar] [CrossRef]
  83. Liu, Y.; Yang, X.; Zhu, S.; Wang, Y. Postharvest application of MeJA and NO reduced chilling injury in cucumber (Cucumis sativus) through inhibition of H2O2 accumulation. Postharvest Biol. Technol. 2016, 119, 77–83. [Google Scholar] [CrossRef]
Ijms 23 10046 g001 550
Figure 1. Endogenous NO production pathway in plants. NO, nitric oxide; NOS, nitric oxide synthase; NR, nitrate reductase; GSNO, S-nitrosoglutathione; GSNOR, S-nitrosoglutathione reductase; NADPH, NADPH oxidase; NADH, Nicotinamide adenine dinucleotide; GSSG, Oxidized glutathione; NH3, Ammonia.
Figure 1. Endogenous NO production pathway in plants. NO, nitric oxide; NOS, nitric oxide synthase; NR, nitrate reductase; GSNO, S-nitrosoglutathione; GSNOR, S-nitrosoglutathione reductase; NADPH, NADPH oxidase; NADH, Nicotinamide adenine dinucleotide; GSSG, Oxidized glutathione; NH3, Ammonia.
Ijms 23 10046 g001
Ijms 23 10046 g002 550
Figure 2. The regulatory mechanisms involving NO that are related to the postharvest senescence of plants: (A) ethylene biosynthesis, (B) the antioxidant system, (C) polyamine metabolism and γ-aminobutyric acid (GABA) shunting. SAM, S-adenosyl-methionine; ACS, 1-aminocyclopropane-1-carboxylate synthase; ACO, ACC oxidase; NO, nitric oxide; SOD, superoxide dismutase; CAT, catalase; POD, peroxidase; GR, Glutathione reductase; NADPH, NADPH oxidase; GSH, glutathione; GSSG, Oxidized glutathione; O−2, Superoxide radicals; H2O2, hydrogen peroxide; Put, putrescine; Spd, spermidine; Spm, spermine; ADC, arginine decarboxylase; DAO, diamine oxidase; PAO, polyamine oxidase; GABA, γ-aminobutyric acid.
Figure 2. The regulatory mechanisms involving NO that are related to the postharvest senescence of plants: (A) ethylene biosynthesis, (B) the antioxidant system, (C) polyamine metabolism and γ-aminobutyric acid (GABA) shunting. SAM, S-adenosyl-methionine; ACS, 1-aminocyclopropane-1-carboxylate synthase; ACO, ACC oxidase; NO, nitric oxide; SOD, superoxide dismutase; CAT, catalase; POD, peroxidase; GR, Glutathione reductase; NADPH, NADPH oxidase; GSH, glutathione; GSSG, Oxidized glutathione; O−2, Superoxide radicals; H2O2, hydrogen peroxide; Put, putrescine; Spd, spermidine; Spm, spermine; ADC, arginine decarboxylase; DAO, diamine oxidase; PAO, polyamine oxidase; GABA, γ-aminobutyric acid.
Ijms 23 10046 g002
Ijms 23 10046 g003 550
Figure 3. Schematic model of the interaction among H2, H2S, H2O2 and other plant hormones in postharvest senescence. (A) NO interacts with ethylene, (B) NO interacts with H2S, H2O2, GATA or OA, (C) NO interacts with plant hormones. AVG, aminoethoxyvinylglycine; 1-MCP, 1-methylcyclopropene; Arg, arginine; OA, oxalic acid; NOS, nitric oxide synthase; ABA, abscisic acid; NO, Nitric oxide; H2S, hydrogen sulfide; H2O2, hydrogen peroxide; MT, Melatonin; MeJA, Methyl jasmonate; GABA, γ-aminobutyric acid; l-/d-CD, 1-/d-cysteine desulfhydrase; OAS-TL, O-acetylserine (thiol)lyase; SiR, sulfite reductase; β-CAS, β-cyanoalanine synthase; JA, jasmonic acid; SA, salicylic acid.
Figure 3. Schematic model of the interaction among H2, H2S, H2O2 and other plant hormones in postharvest senescence. (A) NO interacts with ethylene, (B) NO interacts with H2S, H2O2, GATA or OA, (C) NO interacts with plant hormones. AVG, aminoethoxyvinylglycine; 1-MCP, 1-methylcyclopropene; Arg, arginine; OA, oxalic acid; NOS, nitric oxide synthase; ABA, abscisic acid; NO, Nitric oxide; H2S, hydrogen sulfide; H2O2, hydrogen peroxide; MT, Melatonin; MeJA, Methyl jasmonate; GABA, γ-aminobutyric acid; l-/d-CD, 1-/d-cysteine desulfhydrase; OAS-TL, O-acetylserine (thiol)lyase; SiR, sulfite reductase; β-CAS, β-cyanoalanine synthase; JA, jasmonic acid; SA, salicylic acid.
Ijms 23 10046 g003
Table
Table 1. The effects of NO on postharvest senescence in fruits.
Table 1. The effects of NO on postharvest senescence in fruits.
MaterialsTreatmentStorageEffectsMechanismsReferences
Apple slicesNO fumigation (1 h, 10 μL·L−1)10 °CDelaying postharvest senescence [17]
Apple slicesInfiltration with DETANO solution for 60 sRTDelaying postharvest senescence [18]
Wax appleNO fumigation (2 h, 10 μL·L−1)4 ± 0.5 °CDelaying postharvest senescence [19]
AppleSNP spray (50 μM)18 ± 1 °CDelaying postharvest senescenceEthylene biosynthesis[20]
StrawberryInfiltration with DETANO
Fumigation with NO gas		RTDelaying postharvest senescence [21]
KiwifruitSNP immersion for 10 min (0.2 mM)RTDelaying postharvest senescenceAntioxidant system
Cell wall metabolism		[6]
BlueberriesGSNO solution treatment for 30 min (1 mM)4 °CDelaying postharvest senescenceAntioxidant system[22]
BayberriesNO fumigation (2 h, 20 μL·L−1)1 ± 0.5 °CDelaying postharvest senescence
Alleviating chilling injury		Antioxidant system[23]
KiwifruitsNO fumigation (3 h; 10, 20 and 30 μL·L−1)
NO dip (10 min; 0.5, 1.0 or 2.0 mM)		20 °CDelaying postharvest senescence
Improving postharvest quality		Antioxidant system[24]
MangoSNP immersion (5 min, 1.0 mM or 1.5 mM)8 ± 0.5 °CDelaying postharvest senescence
Alleviating chilling injury		Ethylene biosynthesis[25]
MangoNO fumigation (2 h; 5, 10, 20 and 40 μL·L−1)5 ± 1 °CDelaying postharvest senescence
Improving postharvest quality
Alleviating chilling injury		Ethylene biosynthesis[26]
MangoSNP immersion (5 min, 0.1 mM)25 °CDelaying postharvest senescence
Improving postharvest quality
Inhibiting postharvest diseases		 [27]
BananaSNP immersion (5 min, 0.05 mM)7 °CDelaying postharvest senescence [28]
Banana Delaying postharvest senescence [29]
PistachiosSNP spray (30 s; 15, 30, 45 and 60 μM)2 ± 1 °CDelaying postharvest senescenceAntioxidant system[30]
JujubeNO fumigation (3 h, 20 μL·L−1)0 ± 1 °CDelaying postharvest senescence
Improving postharvest quality		Antioxidant system[31]
LitchiNO dip (5 min; 0.5, 1.0 or 2.0 mM)32 ± 2 °CDelaying postharvest senescence
Improving postharvest quality		 [32]
CherryNO dip (5 min; 0.25, 0.5, 1.0 and 1.5 mM)2 °CDelaying postharvest senescencePolyamine metabolism and GABA shunting[33]
GuavaSNP immersion (5 min; 0.5, 1.0, and 1.5 mM)20 ± 3 °CDelaying postharvest senescence
Improving postharvest quality		Antioxidant system[34]
GrapeSNP immersion (5 min, 0.25 and 0.5 Mm)−0.5 °CDelaying postharvest senescence
Alleviating chilling injury		Antioxidant system[35]
Pointed gourdNO dip (10 min, 1.0 and 2.0 mM)12 °CDelaying postest senescence
Improving postharvest quality		Antioxidant system[36]
PersimmonNO dip (30 min, 1.0 and 1.5 mM)1 °CDelaying postharvest senescenceAntioxidant system[37]
PlumsNO fumigation (3 h; 5, 10 and 20 μL·L−1)21 ± 1 °CDelaying postharvest senescence
Improving postharvest quality, alleviating chilling injury		 [38]
PlumsCold storage Delaying postharvest senescenceCell wall metabolism[39]
PeachNO fumigation (3 h, 10 μL·L−1)4 °CDelaying postharvest senescence
Improving postharvest quality		Sugar metabolism[40]
TomatoSNP immersion (30 min, 1 mM)25 °CDelaying postharvest senescence
Inhibiting postharvest diseases		Ethylene biosynthesis[41]
CitrusSNP immersion (2 min, 2%)20 °CDelaying postharvest senescence
Improving postharvest quality
Inhibiting postharvest diseases		 [42]
PapayaNO fumigation (2 h, 20 μL·L−1)20 °CDelaying postharvest senescenceCell wall metabolism[43]
OrangesNO dip (10 min; 30, 50 and 100 mM)20 °CDelaying postharvest senescence
Improving postharvest quality
Inhibiting postharvest diseases		 [44]
PeachNO fumigation (5 h, 10 μL·L−1)21 ± 1 °CImproving postharvest qualityEthylene biosynthesis[5]
Peach Improving postharvest quality [45]
BananaSNP immersion (5 min, 0.05 mM)22 ± 1 °CImproving postharvest quality
Alleviating chilling injury		Antioxidant system
Energy metabolism		[46]
AppleNO dip (5 min; 50, 100 and 200 µM)25 ± 2 °CImproving postharvest quality
Inhibiting postharvest diseases		Antioxidant system[47]
KiwifruitNO dip (10 min; 0.5, 1 and 2 µM)4 °CImproving postharvest qualityAntioxidant system[48]
Winter jujubeNO fumigation (3 h; 10, 20 and 30 μL·L−1)22 °CImproving postharvest quality [49]
PeachNO fumigation (1 h; 5, 10, 20 and 30 μL·L−1)25 °CImproving postharvest quality [50]
OrangesSNP immersion (5 min, 1 mM)18–23 °CImproving postharvest quality [51]
PeachNO dip (10 min; 0.5, 15 and 100 μM)20 °CInhibiting postharvest diseases [52]
TomatoL-NNA, NaN 3 (0.5 min, 0.1 mM)25 ± 1 °CInhibiting postharvest diseases [53]
PitayaSNP immersion (8 min, 0.1 mM)25 °CInhibiting postharvest diseases Cell wall metabolism[54]
OrangeSNP immersion (5 min, 0.25 or 0.5 mM)3 °CAlleviating chilling injuryAntioxidant system[55]
BananaNO fumigation (3 h, 60 μL·L−1)7 °CAlleviating chilling injuryAntioxidant system[56]
LongkongSNP immersion (20 min; 10, 20 and 30 mM)13 °CAlleviating chilling injuryAntioxidant system[57]
Hami melonNO fumigation (3 h, 60 μL·L)1 + 0.5 °CAlleviating chilling injuryCBF pathway[58]
TomatoNO fumigation (5 h, 200 μL·L−1)20 °C Ethylene biosynthesis[59]
PearSNP immersion (12 h, 100 μM)25 °C Ethylene biosynthesis[60]
Table grapesNO fumigation (300 μL·L−1)1 + 0.5 °C Antioxidant system[3]
BananaSNP immersion (5 min, 0.05 mM)7 °C Polyamine metabolism and GABA shunting[61]
CherrySNP immersion (20 min; 250, 500 and 1000 μM)25 °C Polyamine metabolism and GABA shunting[33]
PeachSNP immersion (10 min, 0.50 μM)4 °C Cell wall metabolism[62]
Raspberries Sugar metabolism[63]
Apple Sugar metabolism[64]
TomatoSNP immersion (0.5 min, 0.05 and 0.1 mM)2 ± 1 °C CBF pathway[65]
PeachGSNO immersion (20 min, 60 μM)23 °C S-nitrosylation[66]
Notes: RT, room temperature; SNP, sodium nitroprusside; DETANO, diethylenetriamine-nitric oxide; GSNO, S-nitrosoglutathione.
Table
Table 2. Overview of the genes regulated by NO during the postharvest storage of fruits.
Table 2. Overview of the genes regulated by NO during the postharvest storage of fruits.
PlantsGenesReferences
Table grapeVvSOD, VvCAT, VvPOD2 and VvGR[3]
BananaMaSOD, MaCAT, MaPOD and MaAPX[56]
KiwifruitPAL, POD and CHT[6]
Wax appleSsC4H[19]
TomatoLeACO1, LeACOH2 and LeACO4[59]
TomatoLeACS2, LeACS4, LeACO1, LePG, LePhy1 and LePME[41]
PearPcCel, PcPG, PcACS, PcACO and PcNOS[60]
TomatoLeCBF1[65]
Hami melonCmCBF1 and CmCBF3[58]
AppleMdSPS, MdSS, MdNI, HK and FK[64]
PeachPpaSPS1/2 PpaAI1[40]
PeachGSNOR PR1, NPR1 and TGA1[66]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Li, C.; Yu, W.; Liao, W. Role of Nitric Oxide in Postharvest Senescence of Fruits. Int. J. Mol. Sci. 2022, 23, 10046. https://doi.org/10.3390/ijms231710046

AMA Style

Li C, Yu W, Liao W. Role of Nitric Oxide in Postharvest Senescence of Fruits. International Journal of Molecular Sciences. 2022; 23(17):10046. https://doi.org/10.3390/ijms231710046

Chicago/Turabian Style

Li, Changxia, Wenjin Yu, and Weibiao Liao. 2022. "Role of Nitric Oxide in Postharvest Senescence of Fruits" International Journal of Molecular Sciences 23, no. 17: 10046. https://doi.org/10.3390/ijms231710046

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