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Review

Molecular and Genetic Events Determining the Softening of Fleshy Fruits: A Comprehensive Review

by
Zhenzhen Peng
1,
Gangshuai Liu
1,
Hongli Li
1,
Yunxiang Wang
2,*,
Haiyan Gao
3,
Tomislav Jemrić
4 and
Daqi Fu
1,*
1
Laboratory of Fruit Biology, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China
2
Institute of Agri-Food Processing and Nutrition, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, China
3
Key Laboratory of Post-Harvest Handing of Fruits, Ministry of Agriculture and Rural Affairs, Food Science Institute, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
4
Department of Pomology, Division of Horticulture and Landscape Architecture, Faculty of Agriculture, University of Zagreb, 10000 Zagreb, Croatia
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2022, 23(20), 12482; https://doi.org/10.3390/ijms232012482
Submission received: 7 August 2022 / Revised: 28 September 2022 / Accepted: 13 October 2022 / Published: 18 October 2022
(This article belongs to the Special Issue Recent Advances in Plant Molecular Science in China 2022)
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Abstract

:
Fruit softening that occurs during fruit ripening and postharvest storage determines the fruit quality, shelf life and commercial value and makes fruits more attractive for seed dispersal. In addition, over-softening results in fruit eventual decay, render fruit susceptible to invasion by opportunistic pathogens. Many studies have been conducted to reveal how fruit softens and how to control softening. However, softening is a complex and delicate life process, including physiological, biochemical and metabolic changes, which are closely related to each other and are affected by environmental conditions such as temperature, humidity and light. In this review, the current knowledge regarding fruit softening mechanisms is summarized from cell wall metabolism (cell wall structure changes and cell-wall-degrading enzymes), plant hormones (ETH, ABA, IAA and BR et al.), transcription factors (MADS-Box, AP2/ERF, NAC, MYB and BZR) and epigenetics (DNA methylation, histone demethylation and histone acetylation) and a diagram of the regulatory relationship between these factors is provided. It will provide reference for the cultivation of anti-softening fruits.

1. Introduction

Fleshy fruits are important sources of human diet due to their rich nutrients such as carbohydrates, vitamins, trace elements and dietary fiber, which are benefit to the health and immunity of human [1]. They are widely cultivated in the world and loved by most consumers. The commercial value of fleshy fruits is affected by their color, nutritional composition, taste, flavor, texture, etc. Among these, fruit softening plays an important role because it is a sign of fruit full ripening marked with ideal color, flavor and accumulation of a large amount of flavor and nutrients and also is conducive to the dispersion and dissemination of fruit seed; however, excessive softening reduces the resistance of fruits to mechanical injury and pathogen infection, resulting in a serious shortening the shelf life and increasing postharvest losses. [2].
Softening that occurs during fruit ripening and postharvest storage includes comprehensive changes in physiology, biochemistry, cell structure and gene expression [3]. It is not only controlled by internal factors (cell wall metabolism, transcriptional regulation, hormone signal transduction, etc.) but also influenced by external environmental conditions (temperature, humidity, light, etc.) [4]. Extensive studies on softening during the ripening stage and postharvest storage of fleshy fruit have been focused on the model climacteric fruit tomato and the non-climacteric fruit strawberry, as well as on several other economically important fruits such as kiwifruit, banana, peach and grape [5]. Strong evidence demonstrates that the ultrastructure and metabolism of cell wall are key factors during the softening of fleshy fruits [6,7,8,9,10]. Fruit softening is considered a process of cell wall polysaccharide modification or breakdown [5,6]. For example, the CRISPR/Cas9-mediated targeted mutagenesis of tomato polygalacturonase genes (SlPG) delays tomato fruit softening [11]. The climacteric fruits require ethylene to start its ripening and softening processes; however, the softening of non-climacteric fruits is more linked to other phytohormones such as abscisic acid and auxin [12,13].
The genetic control of fruit softening increased dramatically by transgenic technology in the last decades [14]. Many transcription factors (LOB1, ERF4, and FSR, etc.) and genes included in phytohormone synthesis and signal transduction (FIS1, SlAREB1, SlBES1, etc.), which are related to fruit softening, have been identified and used to control fruit softening. The silencing of LOB1, FIS1, SlBES1, and PL can enhance fruit firmness and prolong fruit’s shelf life without negative effects on tomato fruit flavor and nutrition [15,16,17,18,19,20,21]. Epigenetic regulation including DNA methylation, histone methylation, and acetylation also is reported to be involved in the ripening and softening of many fruits [4]. DNA methylation is located in a cascade with histone methylation modifications [22,23]. In addition, there is increasing evidence that transcriptional factors (TFs), phytohormones, and epigenetic regulators work together to regulate cell wall metabolism during fruit softening [24,25,26,27]. Here, we summarize advances in cell wall metabolism, phytohormones, transcription factors (TFs), and epigenetics related to fruit softening. It will provide a new strategy for improving fleshy fruit quality by controlling fruit softening in the future.

2. Cell Wall Metabolism and Structure Remodeling

2.1. Cell Wall Structure and Softening-Associated Changes

The cell wall of plants not only functions as the first barrier against pathogen attacks but also as the mechanical support of the plant [28]. It is composed of three layers, including the primary wall, middle lamella and secondary wall. The primary wall is mainly composed of cellulose, hemicellulose, pectin, glycoprotein, etc., and is accompanied by the deposition of polysaccharides during cell expansion. The secondary wall characterized by thickening and lignification contains cellulose, hemicellulose, pectin and lignin [29]. The middle lamella responsible for gluing adjacent cells together is comprises pectin between primary walls [30]. The composition of the cell wall determines the cell structure, resulting in different shapes, sizes and functions of the plant cells [31] (Figure 1A). Usually, the cell wall structure of fruits mainly consists of a parenchyma layer, especially in fleshy fruits at the ripening stage, at only the primary wall and the middle lamella and rarely develops to secondary walls [32]. Fruit softening is accompanied by changes in cell wall ultrastructure and cell wall metabolism, which affect fruit texture [8,25]. The cell wall ultrastructure during fruit softening includes the dissolution of the middle lamella and the gradual disintegration of the fibrous matrix throughout the cell wall, resulting in a decrease in cell adhesion, an increase in cell gaps and a decrease in cell wall thickness and density [33,34,35,36]. Fruit softening is mainly influenced by components and metabolism of the cell wall, which involves the coordination of a number of cell-wall-modifying enzymes and proteins. The fruit’s cell wall is mainly composed of cellulose, hemicellulose and pectin. Cellulose and hemicellulose are interwoven by glycosidic bonds and hydrogen bonds, forming a polysaccharide skeleton as the supporting structure of the cell (Figure 1B). The calcium ion and pectin in the fruit cell wall can form a calcium bridge through a covalent bond to mediate adhesion between cells, resulting in enhancements in cell wall strength and fruit firmness [6,37].

2.2. Roles of Cell Wall Degrading Enzymes on Fruit Softening

Pectin related to fruit softening is a class of polysaccharides consisting of galacturonic acid, homogalacturonans (HGs), rhamnogalacturonan-I (RG-I), rhamnogalacturonan-II (RG-II), xylogalacturonan (XG) and apiogalacturonan(AG)[35]. Pectin can be degraded into soluble pectin and pectate by demethylation during fruit softening, leading to cell wall loosening and disintegration [36]. In addition, metabolism processes of the cell wall components of fruit occurs during fruit softening, such as hemicellulose dissolution and depolymerization, cell wall polysaccharide degradation and the reduction in the esterification degree of pectin and neutral sugar content in pectin. [38,39]. The degradation enzymes related to cell wall metabolism include pectinase, hemicellulose and cellulase, but non-enzymatic pathways are also a factor correlated with fruit softening [40]. Pectin methylesterase (PME), pectin lyase (PL), polygalacturonase (PG), β-galactosidase (β-Gal), xyloglucan endotransglucosylase/hydrolase (XTH) and expansin (EXP) are the major cell-wall-degrading enzymes synergistically involved in cell wall degradation during fruit softening [10,41]. PME randomly hydrolyzes the methylated carboxyl group in polygalacturonic acid to form pectate, the substrate of PG; however, PME can also act on galacturonic acid by a linear block fashion to produce long stretches of negatively charged carboxylates that cross connect with Ca2+, resulting in reduced cell wall porosity and the hardening of the cell wall [42,43]. PL acts on the deesterified polygalacturonic acid to form a double bond between C4 and C5 and finally blocks the α-1,4-glycosidic bond to produce pectin oligosaccharides [44]. PGs are divided into three types: external PGs, internal PGs and rhamnose PGs. Among these, internal PGs participate in the degradation of polygalacturonic acid and pectin in the fruit’s cell walls [45].
In general, the cell wall mainly undergoes the following metabolic reactions related to softening during fruit ripening: PME catalyzes the demethylation of pectin, PL catalyzes the decomposition of deesterified polygalacturonic acid, and PG catalyzes the hydrolysis of α- 1,4-galacturonic acid to produce uronic acid. Fruit softening is dynamically regulated by the above three factors (Figure 1C). The results showed that the silencing of PE1 or PMEU1 in tomato accelerates fruit softening, while the co-silencing of PE2 and PE1 in tomato would completely prevent ripening [46]. The overexpression of FvPME38/39 in strawberries reduces fruit firmness by affecting pectin content and cell wall structure, implying that PME plays a key role in the fruit softening process [43,47]. In apricots, the transcript level of the pectin methylesterase gene PaPME1 elevated with increased storage times [47]. The silencing of PL in tomato and strawberry decreases water-soluble pectin (WSP) content and enhances fruit firmness without affecting other aspects of ripening, while the overexpression of FvPLA accelerates fruit softening in strawberry fruit [7,48]. Similarly, the silencing of PpePL1/15 delays softening by inhibiting the depolymerization of pectin in peach fruit [49]. The overexpression of SlPG49, a newly identified PG gene in tomato fruit, promoted tomato fruit softening, and the silencing of FaPG1 in strawberry enhances the fruit’s firmness by inhibiting cell wall degradation and extends its shelf life [50,51]. In other fleshy fruits such as peach, grapevine, banana and pear, it is reported that their fruit softening is also regulated by PG genes [52,53].
β-Gal catalyzes the hydrolysis of the β-galactoside side chains into pectin during fruit ripening [54]. The silencing of β-galactosidase genes SlTBG4 in tomato or FaβGal4 in strawberry can inhibit fruit softening [55,56]. Genetic analysis in peach revealed that β-gal (encoded by PpBGAL2 and PpBGAL16) is responsible for cell wall degradation during fruit softening [57], and silencing PpBGAL10 and PpBGAL16 by virus-induced gene silencing (VIGS) delayed fruit softening of peach [58]. XTHs (xyloglucan endotransglucosylase/hydrolase) catalyses xyloglucan endohydrolysis (XEH) and/or endotransglycosylation (XET) are involved in the modification of cell wall structure by cleaving and, often, are also involved in re-joining xyloglucan molecules in primary plant cell walls [59] (Figure 1D). The transient overexpression of MdXTHB gene in ‘Golden Delicious’ and ‘Fuji’ apples promotes apple fruit softening, and the transient overexpression of FvXTH9 and FvXTH6 in strawberries resulted in faster fruit ripening [60,61]. In addition, both DkXTH6 and DkXTH7 have been shown to play important roles in the softening process of persimmon fruits during storage. DkXTH6 induces persimmon fruit softening by participating in cell wall recombination and loosening, while DkXTH7 can maintain the firmness of mature fruit by participating in cell wall synthesis [62]. There is evidence that a reduction in XET activity during ripening may contribute to fruit softening. The overexpression of SlXTH1 in tomatoes delays fruit softening in transgenic tomatoes [63].
Expansin (EXP), a plant cell wall expansin protein, can break the chemical bond between microfibrils and glucans by binding to glucan-coated cellulose, which makes cellulose’s surface glucans susceptible to cellulases, resulting in fruit cell wall loosening [64] (Figure 1D). EXPs are associated with fruit softening and have different expression patterns in tomato, strawberry, banana and other fleshy fruits [65,66,67]. The silencing of LeEXP1 in tomatoes enhances fruit firmness and extends its shelf life, while the co-silencing of LeEXP1 and LePG further inhibited fruit softening [68,69]. The expression levels of PsEXPA10 and FaEXPA2/5 increased significantly during the softening of plum and strawberry fruits [70,71,72]. In addition, pectin acetylesterase (PAE) is also involved in fruit softening. For example, the overexpression of MdPAE10 encodes pectin acetylesterase and leads to a significant reduction in flesh firmness. In contrast, silencing MdPAE10 delays the decline of fruit firmness [73]. FaEG1 genes encoding endo-β-1, 4-glucanase are reported to be involved in the breakdown of cellulose and hemicellulose structures and play a role in cell wall restructuration during strawberry fruit softening [74]. In summary, the cell wall metabolism related to fruit softening is delicate and complex, including a variety of enzymes related to cell wall metabolism, as shown in Table 1.
Ijms 23 12482 g001 550
Figure 1. Cell wall structure. (A) Schematic representation of the cell wall structure of three cells; (B) schematic representation of the structural components of the cell wall (after Farinati et al. [75]); (C) schematic representation of the pectin structure. Pectin is composed of five different types of polysaccharides, and various pectin-degrading enzymes are involved in pectin degradation (see text); (D) The cross-linking structure of hemicellulose and cellulose microfibril, EXP and XTH are involved in the depolymerization of the structure.
Figure 1. Cell wall structure. (A) Schematic representation of the cell wall structure of three cells; (B) schematic representation of the structural components of the cell wall (after Farinati et al. [75]); (C) schematic representation of the pectin structure. Pectin is composed of five different types of polysaccharides, and various pectin-degrading enzymes are involved in pectin degradation (see text); (D) The cross-linking structure of hemicellulose and cellulose microfibril, EXP and XTH are involved in the depolymerization of the structure.
Ijms 23 12482 g001

3. Phytohormones Regulation of Fruit Softening

Phytohormones play an important role in fruit development and ripening. such as ethylene (ETH), abscisic acid (ABA), auxin (IAA), and brassinosteroid (BR), etc. For example, the ripening and softening of climacteric fruits depend on the production of a large amount of ethylene, while non-climacteric fruits depend on ABA to start their fruit ripening and softening processes [76].

3.1. ABA

ABA regulates fruit softening in the upstream signaling pathway of ethylene [77]. For example, ABA promotes ETH production to reduce pectinesterase activity, which accelerates fruit pulp softening during mango fruit ripening [78]. The overexpression of the lycopene β-cyclase gene (LCYb) in tomato results in increased levels of β-carotene (provitamin A), a precursor of ABA. The increased ABA level leads to a reduction in ethylene production; an increase in cell density; the thickening of the fruit’s cuticle; the down-regulation of PG1, PL and EXP1 genes; and the up-regulation of PMEU1/2, which finally delays fruit softening and prolongs the fruit’s shelf life [79]. The silencing of SlNCED1-encoding 9-cis-epoxycarotenoid dioxygenase (NCED) in the biosynthesis of ABA results in the down-regulation of cell wall metabolism gene (SlPG, SlPME, SlTBG, SlXET, SlCELs and SlEXP) expression and inhibits fruit softening [80]. On the other hand, ABA can induce changes in the transcription level of genes encoding cell-wall-degrading enzymes. For example, exogenous treatments with ABA can accelerate strawberry fruit softening by dramatically promoting the accumulation of transcripts of cell wall metabolism genes such as FcPG, FcRGL1 and FcEXP5 [81]. Moreover, the overexpression and repression of SlPYL9, encoding the ABA receptor, can accelerate or delay fruit softening and pericarp thickness by affecting the transcription of cell wall modification genes (SlPG and SlEXP6) [82]. Treatments with ABA can cause the postharvest softening of blueberry fruits by inducing the expression of VcPEs, VcPGs, VcCx and VcGal [83]. The silencing of PacCYP707A2, which encodes the ABA degradation enzyme in sweet cherries, promotes the accumulation of ABA and the up-regulation of PacNCED1 transcript levels, resulting in the up-regulation of PacACO1 and a reduction in fruit firmness [84].

3.2. ETH

Ethylene is the first-known plant hormone involved in fruit softening. Numerous studies have shown that ETH promotes the softening of climacteric fruits, and the process of fruit softening is influenced by ETH synthesis, distribution, signal transduction and downstream genes. The peak of ethylene production during fruit ripening is necessary for the ripening of climacteric fruit fruits, such as tomatoes, kiwifruit, apricots and plums. For example, exogenous treatments with ETH can rapidly reduce the firmness of kiwifruit and strawberry fruit by inducing CkPGC and FaPG1 gene expressions [85,86]. ETH treatments also accelerated the softening of papaya and apricot fruits due to cell wall decompositions, while ethylene receptor inhibitor (1-methylcyclopropene, 1-MCP) can delay fruit softening by inhibiting the expression of genes related to cell wall degradation [87,88]. The silencing of the genes of key enzymes of system II ethylene biosynthesis in tomatoes, such as SlACS2, SlACS4, SlACO1 and SlACO3, significantly inhibited fruit softening [89]. ETH receptors are negative regulators of ethylene signal transduction, and it was found that tomato fruit with LeETR4 or LeETR6 single mutants exhibited high sensitivity to ETH, and exogenous ETH treatments could rapidly degrade LeETR4 or LeETR6 via the 26s protease pathway to regulate tomato ripening [90,91]. The LeEIN2 gene is a positive regulator of the ETH signaling pathway. The silencing of LeEIN2 significantly inhibits fruit softening by the down-regulation of softening-related genes (PG, E4 and TomLoxB) [92,93].

3.3. IAA

In addition, genes encoding DNA demethylases are inhibited by IAA to maintain high methylation levels in the fruit, which inhibits the ripening process [94,95]. PpYUC11, a key gene involved in IAA biosynthesis, regulates IAA levels at the later stage of peach ripening and also is a candidate gene for regulating peach fruit softening [96]. PpIAA1 in peach can bind to the PpACS1 promoter to activate its expression. The overexpression of PpIAA1 in tomato accelerates fruit ripening and shortens fruit shelf life by increasing the production of ETH and controlling the expression of ripening-related genes [97]. On the other hand, the overexpression of the IAA-responsive gene PpSAUR43 down-regulates the cell wall degradation gene PpPG and delays the softening of peach fruit [98]. In kiwifruit, the silencing of AcGH3.1, a gene controlling IAA homeostasis, increased fruit firmness during ripening and delays fruit softening during postharvest storage. The expression of AcGH3.1 was also induced by 1-naphthylacetic acid (NAA, IAA analogue) [99]. The application of exogenous IAA in grapes inhibits the accumulation of ABA and suppressed the expression of softening-related genes, such as PE, PG, PL and CELL, which delayed fruit ripening and softening [100]. Similarly, exogenous IAA reduced the transcription level of genes encoding pectate lyase, β-D-xylosidase, endoglucanase, β-galactosidase and endo-1,3-β-glucosidase in strawberry and promoted the cellulose-xyloglucan framework’s reorganization by activating the expression of XT1 and XTH, which delayed the softening of fruits during postharvest storage, [101].

3.4. BR

BRs are a group of steroid hormones involved in plant growth and development [102]. Recent studies have shown that BRs have an effect on fruit ripening. For example, exogenous brassinolide treatments of tomato promoted fruit softening by increasing the production of ETH, as did persimmon and banana fruits [103,104,105]. The overexpression of SlCYP90B3 gene involved in brassinosteroid biosynthesis delays fruit softening by up-regulating ETH biosynthesis (SlACS2/4 and SlACO1) and signaling (SlETR3 and SlCTR1) in tomato fruits. However, silencing SlCYP90B3 inhibits the softening of tomato fruit [106]. MaBZR1 and DkBZR2 involved in BR signaling mediated fruit softening by regulating genes involved in ETH biosynthesis and cell wall degradation in bananas and persimmons. The transient overexpression of DkBZR2 in persimmons promotes the conversion of acid-soluble pectin to WSP and increases ETH production in fruits [104,107].

3.5. Other Phytohormones

In addition to ETH, ABA, IAA and BRs, gibberellins (GA), jasmonic acid (JA) and salicylic acid (SA) are also involved in fruit softening. A mutant of FIS1 gene encoding GA2-oxidase increased the level of bioactive gibberellins and enhanced the accumulation of cutin and wax by regulating the expression of cuticle accumulation and deposition-related genes (CYP86A69, CYP77A-LIKE, GDSLs and CERs), which increased fruit firmness and shelf life without adverse effects on fruit weight or flavor. It will provide a potential strategy for tomato breeders to cultivate varieties resistant to softening [18]. The exogenous treatment of strawberries and grapes with JA induced fruit softening by promoting the expression of genes involved in cell wall metabolism. The transient overexpression of FaAOC and FaAOS, two key genes involved in jasmonic acid synthesis, accelerated strawberry fruit softening [108,109]. Treatment with SA effectively delayed fruit firmness decline in tomato by strongly inhibiting the expression of ETH biosynthesis genes (ACO1 and ACS2) and reducing the activity of cell-wall-degrading enzymes [110]. In summary, the softening process is controlled by phytohormones and also involves the co-regulation of other factors (Figure 2). The complex molecular mechanism of phytohormone-regulating fruit softening has not been fully understood, and it needs to be better investigated.

4. Transcriptional Regulation of Fruit Softening

Although different tissues of the same organism contain the same genomic DNA, the transcription of each gene is time- and space-specific. For example, tomato fruit is green and hard at the immature stage, whereas it becomes red and soft at the ripening stage due to the spatiotemporal expression specificity of genes related to ripening and softening. The transcription of genes is regulated by transcription factors. Transcription factors can bind to the promoter region of target genes to activate or inhibit their transcriptional factor. Fruit softening occurs during fruit ripening and is regulated by several transcription factors related to fruit softening. Currently, many transcription factors related to softening have been isolated and verified.

4.1. MADS-Box TFs and Fruit Softening

RIN (ripening inhibitor) is an important MADS-Box TF involved in all aspects of fruit ripening and directly targets many ripening-related genes (PG, TBG4, EXP1, CEL2, etc.). Compared to the wild tomato fruit, the fruit of ripening inhibitor (rin), a tomato natural ripening mutant, softens slowly and has a long shelf life [110]. SlMBP8, MADS-Box TFs, has also been reported to play an important role in fruit softening. Silencing SlMBP8 significantly induced the expression of cell wall metabolism genes such as PG, EXP, HEX, TBG4, XTH5 and XYL and increased the production of ETH by activating the expression of ETH-related genes, resulting in faster water loss and lower storage tolerance in fruits [111]. FRUITFULL homologs (FULs), MADS-Box TFs, also interact with RIN, and the simultaneous silencing of FUL1 and FUL2 delays fruit ripening and reduces the production of ETH and the thickness of the fruit peel’s cuticle, resulting in the inhibition of fruit softening [112,113]. The silencing of MaMADS1 or MaMADS2 in banana delays ripening and softening by inhibiting ETH synthesis [114]. The silencing of PrupeSEP1, a member of the MADS-box TF subfamily, delays fruit softening in melting flesh peaches, and the expression levels of softening-related genes such as ACS2, EIN2, PME1, Endo-PG3, ACO1, ETR2, β-Hex2 and Lox1 were significantly reduced [115]. The silencing of PrupeFUL4 in peach fruit also delayed fruit softening and significantly suppressed the expression of PrupACO1 and PrupACS2, whereas the overexpression of PrupeFUL4 accelerated fruit softening by significantly up-regulating PrupeACO1 [116]. PaMADS7 activates PaPG1 expression by directly binding to the PaPG1 promoter involved in fruit softening in sweet cherries, and the silencing of PaMADS7 in sweet cherry inhibits fruit softening [117].

4.2. AP2/ERF TFs and Fruit Softening

AP2/ERF, a superfamily TFs in plants, is not only involved in fruit ripening but also can regulate the biosynthesis of phytohormones and involved in hormone signaling [118]. AP2a, a member of the AP2/ERF family, negatively regulates ethylene production, and the silencing of AP2a in tomato promotes ETH production and fruit softening [119]. The overexpression of SlERF.B3 genes in tomato accelerates tomato fruit softening by up-regulating the key PG2a gene [120]. A recent study showed that SlERF.F12, a negative regulator of tomato ripening, forms a triplex with TPL2-HDA1/3, and its overexpression suppresses the expression of ripening-related genes ACS2, ACS4, PG2a and PL, which delays fruit softening and prolonging shelf life [121]. PpERF4 in peach activates the transcription of PpACO1 and PpIAA1 genes by binding to their promoters. PpIAA1 interacts with PpPRF4 to form a complex, which activates the transcription of ABA biosynthesis genes (PpNCED2/3) and fruit-softening genes (PpPG1), and ultimately regulates peach fruit ripening and softening by integrating IAA and ETH signals [97]. Recently, Cheng et al. [122] found that PpERF/ABR1 directly binds to the PpPG promoter to activate its expression, which also induces peach fruit softening, and the overexpression of PpERF/ABR1 promotes the production of ETH in accelerating fruit softening. CpERF9 [123], MdERF4 [16] and MaERF11 [124] repress the transcription of cell wall degradation genes during the ripening of papaya, apple and banana.

4.3. NAC TFs and Fruit Softening

NAC proteins are involved in a variety of life processes as plant-specific TFs. Several researchers have shown that NAC proteins positively regulate tomato fruit ripening. For example, silencing SNAC4 in tomatoes maintains fruit firmness and reduces the accumulation of ABA during fruit ripening. SNAC4 directly binds to the promoter regions of SAPK3, SlCYP707A1, SlACS8 and SlACO6 to activate their transcription, which are involved in the synthesis of ABA and ETH and their signal transduction [125]. Gao et al. also found that cell wall degradation genes SlPG2a, SlPL, SlCEL2 and SlEXP1 are targets of NOR-like1, which affects fruit softening by regulating pectin solubilization, cellulose-hemicellulose skeleton depolymerization and cell wall loosening [126]. Subsequently, it was found that NOR, a homolog of NOR-like1, can also bind to the promoter of SlPL and activate its transcription, and the softening of nor mutant fruit is inhibited, while fruit softening is accelerated when NOR was overexpressed [127]. The overexpression of another NAC TF, SlNAC1, in tomato leads to a reduction in fruit firmness and peel thickness and produces more ABA than wild types [128]. Recently, a mutation of NOR by gene editing in melon was found to prevent normal fruit softening, significantly suppressing ETH and ABA production and ultimately extending the shelf life of melon fruits [129]. MaNAC1 and MaNAC2 negatively regulate the ethylene synthesis of banana fruit through MaXB3-mediated ubiquitination degradation pathways, resulting in the inhibition of the softening of banana fruits [130]. FcNAC1, a strawberry fruit ripening-related TF can bind to the FcPL promoter to activate its expression, which was involved in pectin metabolism during strawberry fruit softening [131]. Moreover, the silencing of FaRIF (FaNAC035) enhances fruit firmness by down-regulating the expression of cell wall degradation (FaXYL3 and FaPL3/4) and modification-related genes (FaEXP1/2/3 and FaPME39) [132].

4.4. MYB TFs and Fruit Softening

MYB TFs are a superfamily of TFs in plants. MYB TFs numbering 140 and 110 have been identified, respectively, in tomato and strawberry fruits, and some of these play important roles in cell wall’s metabolism, secondary metabolism and stress response [133]. In tomatoes, SlMYB70, a transcription suppressor, can bind to the promoters of SlACS2 and SlACO3 genes to inhibit their transcription. Silencing SlMYB70 promotes ethylene production to accelerate fruit ripening and softening [89]. In addition, the overexpression of SlMYB75 prolongs tomato fruit shelf life by directly down-regulating the expression of SlFSR, which regulates the transcription of genes related to cell wall modification [134]. The transient overexpression of FvMYB79 in strawberry significantly increases the transcriptional level of FvPME38, resulting in fruit softening and ripening, while silencing FvMYB79 delays fruit ripening and increases fruit firmness [135].

4.5. BZR TFs and Fruit Softening

The BRASSINAZOLE RESISTANT(BZR) TF is a key component of the brassinosteroid signaling pathway. Recently, SlBES1 in tomato was found to contain the BZR structural domain and to be involved in the fruit softening process. SlBES1 directly binds to the PMEU1 promoter and inhibits its expression, and the CRISPR-Cas9 knockout of SlBES1 increases fruit firmness and prolongs its shelf life without affecting fruit nutritional quality [20]. As a transcriptional inhibitor, Banana MaBZR1/2 can directly inhibit ETH biosynthesis and fruit softening by binding to the promoter of ethylene biosynthesis-related genes (MaACS1, MaACO13 and MaACO14) and cell wall modification genes (MaEXP2, MaPL2 and MaXET5). [136].

4.6. Relationship between Other Transcription Factors and Softening

In addition to the ripening-related TFs associated discussed above, silencing SlFSR, a member of GRAS TF family TFs, decreases the expression level of several genes related to cell wall modifications, such as PG, TBG, CEL and XYL, resulting in extending the shelf life of tomato fruits [17]. The transient overexpression of ARF TF CpARF2 in papaya decreases fruit firmness, while the transient silencing of CpARF2 increases fruit firmness, and the ectopic overexpression of CpARF2 in tomato also decreases fruit firmness and induces the production of ETH in the transgenic lines [137]. SlLOB1, a tomato LATERAL ORGAN BOUNDARIES TF, can activate the transcription of EXP1, CEL2, XY, AGP2, TBL, E6 and PL gene in vitro, and the overexpression of SlLOB1 induces cell wall gene expression and promotes fruit softening, while the inhibition of its expression delays fruit softening [15]. The WRKY protein plays a key role in regulating growth, development and plant responses to biological and abiotic stresses. Recently, it was found that the overexpression of FvWRKY48 in strawberries accelerates fruit ripening and increases the level of high galacturonic acid degradation in the pectin cell wall polymer of the middle lamella and three cell junction regions in the fruit. FvWRKY48 can bind to the FvPLA promoter and promote pectin acid lyase activity, accelerating pectin degradation and fruit softening [48]. In banana, MabZIP74 inhibits the expression of the ETH biosynthesis genes, such as MaACO1 and MaACO4 [138]. The expression of bHLH TFs MaTCP5, MaTCP19 and MaTCP20 were all induced by ETH. MaTCP5 and MaTCP20 are transcriptional activators. MaTCP19 is a transcriptional repressor. MaTCP5 and MaTCP20 activate the transcription of MaXTH10/11 involved in fruit softening during banana ripening. MaTCP19 represses its transcription by directly binding to the promoter. More importantly, MaTCP20 interacts synergistically or antagonistically with MaTCP5 or MaTCP19 to enhance or attenuate the transcription of MaXTH10/11 [139].
As mentioned above, different types of transcription factors are involved in fruit softening. (Table 2).

5. Epigenetic Modifications of Fruit Softening

In recent years, substantial evidence has emerged, supporting that epigenetic regulation is an important factor in controlling agronomic traits [141]. The epigenetic modification includes DNA methylation, post-translational histone modification, chromatin remodeling and so on. In addition to TFs and phytohormones, epigenetic regulation plays an essential role in fruit growth, development and ripening (Figure 3).

5.1. DNA Methylation Affects Fruit Softening

DNA methylation is a biological process by which methyl groups are added to the DNA molecule. Methylation can change the activity of a DNA segment without changing the sequence. When methyl groups are located in a gene promoter, DNA methylation typically acts to repress gene transcription [142]. During fruit development and ripening, the methylation and demethylation levels of genome occur dynamically. The researcher found that the reduction in methylation is associated with fruit ripening. Hadfield et al. reported that reduced DNA methylation of highly expressed genes in tomato fruit coincided with the onset of ripening [143]. However, the first evidence that DNA methylation affects tomato softening was a map-cloning of the gene at the COLORLESS NON-RIPENING (CNR) locus, a spontaneous mutation in cnr; the cnr mutant has hypermethylation in its promoter region, but its coding region is normal. The ripening, softening and carotenoid accumulation of the cnr mutant tomato fruit are significantly inhibited [144]. Genome-wide methylation analysis showed the reduction in methylation levels of genes related to fruit ripening and softening such as ACO1, ACS2, PG, PMEU1, RIN, NOR, CNR and TAGL1 during the ripening of tomato fruits [145]. Later, Liu et al. [146] found that the degree of the promoter methylation of genes was related to their expression, while demethylation is catalyzed by demethylase such as DML, SlDML2 in tomato, which is involved in the regulation of fruit ripening and softening. The knockdown or knockout of SlDML2 up-regulates the expression of genes related to coloration, flavor synthesis, synthesis and signaling of ETH and cell wall hydrolysis, resulting in the delay of tomato fruit ripening and softening [147]. DNA methylation also can target SlALKBH2-encoding RNA demethylase to regulate the m6A methylation of mRNA. Delays in the fruit ripening of the SlALKBH2 mutant may be a result of the feedback regulation of SlDML2 stability [148]. Recent studies have shown that SlHMGA3 encoding High-Mobility Group (HMG) A proteins can bind to the SlDML2 promoter and activate its expression, resulting in the promoter DNA methylation of ripening-related TFs regulating ETH biosynthesis and signal transduction [149].

5.2. Histone Demethylation Modification during Fruit Softening

The post-translational modification of histones regulates gene expression by affecting chromatin structure. Reversible covalent modifications of histones include methylation, acetylation, phosphorylation and ubiquitination. SlJMJ6 encoding a histone H3K27me2/3 demethylase in tomato was found to be a positive regulator of fruit ripening by directly activating the transcription of genes related to ripening such as genes for the synthesis of ETH (ACS4, ACO1, etc.) and genes related to fruit softening (PL and TBG4) to reduce their H3K27me3 levels; its overexpression accelerates tomato fruit ripening and softening [150]. Nevertheless, SlJMJ7, an H3K4 demethylase, is a critical negative regulator of fruit ripening in tomato. Overexpressing SlJMJ7 represses the expression of target genes by removing the H3K4me3 of genes related to cell wall modification (CEL2, XTH5, EXP1, XYL1, PG2a, TBG4 and PL1/2/8), ETH biosynthesis-related genes (ACS2/4/8 and ACO6) and transcriptional regulators (RIN, NOR and CNR). SlJMJ7 also directly represses SlDML2 expression by H3K4me3 demethylation during fruit ripening [22].

5.3. Roles of Histone Acetylation in Fruit Softening

Histone deacetylases (HDACs) also affect the expression of genes involved in tomato fruit development and ripening. For example, SlHDA1 and SlHDA3 encode the histone deacetylase, silencing SlHDA3 to induce the expression of genes related to ETH synthesis and cell wall metabolism, which accelerates fruit ripening and softening. [151,152]. Silencing SlHDT3 gene-encoding histone deacetylase delays fruit softening by down-regulating the expression of genes related to fruit cell wall metabolism (HEX, MAN, TBG4, XTH5 and XYL) [153]. PRC2 is responsible for the trimethylation of histone H3 at Lys27. Silencing the SlEZ2 gene encoding the PRC2 protein Zeste enhancer (E(z)) accelerates fruit softening, [154,155].
Epigenetic modifications also are observed during the ripening and softening of other fleshy fruits. In strawberries, DNA methylation levels were reduced during its ripening. At the same time, DNA methyltransferase genes (FvDRM1.3 and FvDRM3.1) were down-regulated, and genes related to photosynthesis and cell wall synthesis were inhibited [156]. Hu et al. [157] also found that MdHDA19 promotes the production of ETH by H3K9 deacetylation in apples, and the silencing of MdHDA19 resulted in decreased fruit firmness. MaHDA1 gene-encoding histone deacetylase in bananas negatively regulates the expression of ripening-related genes during fruit ripening by interacting with TF MaERF11 [124]. The histone deacetylase 2-like gene (DlHD2) may interact with the ETH response factor-like gene (DlERF1) to regulate gene expressions related to fruit senescence [158].

6. Conclusions and Perspectives

Fruit softening is a complex process regulated by cell wall metabolism-related en-zymes, phytohormones, TFs and epigenetics, all four of which interact with each other and synergistically regulate fruit softening. This review summarizes recent advances on the effects of various regulatory factors on fruit softening. The cell wall has been consid-ered a major factor in fruit softening for a long period of time, where several proteins are coordinated and interdependent for cell wall metabolism and modification. As endogenous substances in the fruit, phytohormones play an important role in fruit development and ripening, and ETH and ABA are particularly involved in fruit softening after ripening. In addition, ETH interacts with other phytohormones such as IAA and ABA to regulate the expression of genes related to cell wall metabolism to regulate fruit softening. TFs regulate the expression of downstream target genes related to fruit ripening and softening. More importantly, the study of epigenetic modifications in fleshy fruits, epigenetic markers associated with fruit texture traits and the distribution of DNA methylation may identify important new targets for plant breeding and crop improvement. The epigenetic regulation of fruit ripening is an area that deserves intensive research, providing great potential for fruit quality improvement and breeding. However, fruit softening is more complex than expected, and more research is needed to fill the gaps. For example, the questions are about the role of secondary metabolites produced during fruit ripening in fruit softening and how they coordinate with fruit softening to obtain beneficial nutrients for humans. The contribution of cell wall modifications to fruit softening is not fully understood and the exact role of cell wall structural changes in fruit softening needs further elucidation. Interaction evidence between TFs and ripening-related proteins during fruit ripening is incomplete, especially for fruit softening-related effectors. The establishment of linkage networks between TFs and phytohormones by hormone-related regulatory factors needs to be enriched. Epigenetic alleles of epigenetic modifications need to be explored using techniques such as gene editing to obtain superior cultivars that do not affect postharvest fruit quality but extend fruit shelf life.

Author Contributions

Conceptualization, investigation, visualization, writing—original draft and writing—review and editing, Z.P.; supervision, conceptualization and writing—review and editing, D.F. and Y.W.; writing—review and editing, T.J., H.G., G.L. and H.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Beijing Innovation Consortium of Agriculture Research System (BAIC04-2022) and the National Natural Science Foundation of China (NSFC 31901732, 32072277).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

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

Acknowledgments

The authors thank researchers at the College of Food Science and Nutritional Engineering, China Agricultural University for their help: Benzhong Zhu and Hongliang Zhu for their discussion and suggestions for this manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Giovannoni, J.J. Genetic regulation of fruit development and ripening. Plant Cell 2004, 16, S170–S180. [Google Scholar] [CrossRef] [Green Version]
  2. Seymour, G.B.; Chapman, N.H.; Chew, B.L.; Rose, J.K.C. Regulation of ripening and opportunities for control in tomato and other fruits. Plant Biotechnol. J. 2013, 11, 269–278. [Google Scholar] [CrossRef]
  3. Shi, Y.; Li, B.; Su, G.; Zhang, M.; Grierson, D.; Chen, K. Transcriptional regulation of fleshy fruit texture. J. Integr. Plant Biol. 2022, 64, 1649–1672. [Google Scholar] [CrossRef]
  4. Giovannoni, J.; Nguyen, C.; Ampofo, B.; Zhong, S.; Fei, Z. The epigenome and transcriptional dynamics of fruit ripening. Annu. Rev. Plant Biol. 2017, 68, 61–84. [Google Scholar] [CrossRef]
  5. Li, X.; Xu, C.; Korban, S.S.; Chen, K. Regulatory mechanisms of textural changes in ripening fruits. Crit. Rev. Plant Sci. 2010, 29, 222–243. [Google Scholar] [CrossRef]
  6. Wang, D.; Yeats, T.H.; Uluisik, S.; Rose, J.K.C.; Seymour, G.B. Fruit softening: Revisiting the role of pectin. Trends Plant Sci. 2018, 23, 302–310. [Google Scholar] [CrossRef]
  7. Wang, D.; Samsulrizal, N.H.; Yan, C.; Allcock, N.S.; Craigon, J.; Blanco-Ulate, B.; Ortega-Salazar, I.; Marcus, S.E.; Bagheri, H.M.; Perez Fons, L.; et al. Characterization of CRISPR mutants targeting genes modulating pectin degradation in ripening tomato. Plant Physiol. 2019, 179, 544–557. [Google Scholar]
  8. Vicente, A.R.; Saladié, M.; Rose, J.K.; Labavitch, J.M. The linkage between cell wall metabolism and fruit softening: Looking to the future. J. Sci. Food Agric. 2007, 87, 1435–1448. [Google Scholar] [CrossRef]
  9. Zhang, W.D.; Guo, M.R.; Yang, W.T.; Liu, Y.X.; Wang, Y.; Chen, G.G. The role of cell wall polysaccharides disassembly and enzyme activity changes in the softening process of hami melon (Cucumis melo L.). Foods 2022, 11, 841. [Google Scholar] [CrossRef]
  10. Brummell, D.A.; Harpster, M.H. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol. Biol. 2001, 47, 311–339. [Google Scholar] [CrossRef]
  11. Nie, H.; Shi, Y.; Geng, X.; Xing, G. CRISRP/Cas9-mediated targeted mutagenesis of tomato polygalacturonase gene (SlPG) delays fruit softening. Front. Plant Sci. 2022, 13, 729128. [Google Scholar] [CrossRef] [PubMed]
  12. Liu, Y.; Tang, M.; Liu, M.; Su, D.; Chen, J.; Gao, Y.; Bouzayen, M.; Li, Z. The molecular regulation of ethylene in fruit ripening. Small Methods 2020, 4, 1900485. [Google Scholar] [CrossRef]
  13. McAtee, P.; Karim, S.; Schaffer, R.; David, K. A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front. Plant Sci. 2013, 4, 79. [Google Scholar] [CrossRef] [Green Version]
  14. Atkinson, R.G.; Schröder, R. Genetics of fruit softening. In The Kiwifruit Genome; Springer: Cham, Switzerland, 2016; pp. 205–217. [Google Scholar]
  15. Shi, Y.; Vrebalov, J.; Zheng, H.; Xu, Y.; Yin, X.; Liu, W.; Liu, Z.; Sorensen, I.; Su, G.; Ma, Q. A tomato LATERAL ORGAN BOUNDARIES transcription factor, SlLOB1, predominantly regulates cell wall and softening components of ripening. Proc. Natl. Acad. Sci. USA 2021, 118, e2102486118. [Google Scholar] [CrossRef]
  16. Hu, Y.; Han, Z.; Sun, Y.; Wang, S.; Wang, T.; Wang, Y.; Xu, K.; Zhang, X.; Xu, X.; Han, Z. ERF4 affects fruit firmness through TPL4 by reducing ethylene production. Plant J. 2020, 103, 937–950. [Google Scholar] [CrossRef]
  17. Zhang, L.; Zhu, M.; Ren, L.; Li, A.; Chen, G.; Hu, Z. The SlFSR gene controls fruit shelf-life in tomato. J. Exp. Bot. 2018, 69, 2897–2909. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Li, R.; Sun, S.; Wang, H.; Wang, K.; Yu, H.; Zhou, Z.; Xin, P.; Chu, J.; Zhao, T.; Wang, H.; et al. FIS1 encodes a GA2-oxidase that regulates fruit firmness in tomato. Nat. Commun. 2020, 11, 5844. [Google Scholar] [CrossRef]
  19. Mou, W.; Li, D.; Luo, Z.; Li, L.; Mao, L.; Ying, T. SlAREB1 transcriptional activation of NOR is involved in abscisic acid-modulated ethylene biosynthesis during tomato fruit ripening. Plant Sci. 2018, 276, 239–249. [Google Scholar] [CrossRef]
  20. Liu, H.; Liu, L.; Liang, D.; Zhang, M.; Jia, C.; Qi, M.; Liu, Y.; Shao, Z.; Meng, F.; Hu, S. SlBES1 promotes tomato fruit softening through transcriptional inhibition of PMEU1. Iscience 2021, 24, 102926. [Google Scholar] [CrossRef]
  21. Uluisik, S.; Chapman, N.H.; Smith, R.; Poole, M.; Adams, G.; Gillis, R.B.; Besong, T.; Sheldon, J.; Stiegelmeyer, S.; Perez, L. Genetic improvement of tomato by targeted control of fruit softening. Nat. Biotechnol. 2016, 34, 950–952. [Google Scholar] [CrossRef] [Green Version]
  22. Ding, X.; Liu, X.; Jiang, G.; Li, Z.; Song, Y.; Zhang, D.; Jiang, Y.; Duan, X. SlJMJ7 orchestrates tomato fruit ripening via crosstalk between H3K4me3 and DML2-mediated DNA demethylation. New Phytol. 2022, 233, 1202–1219. [Google Scholar] [CrossRef] [PubMed]
  23. Li, X.; Wang, X.; Zhang, Y.; Zhang, A.; You, C. Regulation of fleshy fruit ripening: From transcription factors to epigenetic modifications. Hortic. Res. 2022, 9, c13. [Google Scholar] [CrossRef] [PubMed]
  24. Kumar, R.; Khurana, A.; Sharma, A.K. Role of plant hormones and their interplay in development and ripening of fleshy fruits. J. Exp. Bot. 2014, 65, 4561–4575. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Forlani, S.; Masiero, S.; Mizzotti, C. Fruit ripening: The role of hormones, cell wall modifications, and their relationship with pathogens. J. Exp. Bot. 2019, 70, 2993–3006. [Google Scholar] [CrossRef]
  26. Song, C.; Shan, W.; Kuang, J.; Chen, J.; Lu, W. The basic helix-loop-helix transcription factor MabHLH7 positively regulates cell wall-modifying-related genes during banana fruit ripening. Postharvest Biol. Technol. 2020, 161, 111068. [Google Scholar] [CrossRef]
  27. Moya-León, M.A.; Mattus-Araya, E.; Herrera, R. Molecular events occurring during softening of strawberry fruit. Front. Plant Sci. 2019, 10, 615. [Google Scholar] [CrossRef] [Green Version]
  28. Chen, Y.; Zhang, S.; Lin, H.; Lu, W.; Wang, H.; Chen, Y.; Lin, Y.; Fan, Z. The role of cell wall polysaccharides disassembly in Lasiodiplodia theobromae-induced disease occurrence and softening of fresh longan fruit. Food Chem. 2021, 351, 129294. [Google Scholar] [CrossRef]
  29. Lampugnani, E.R.; Khan, G.A.; Somssich, M.; Persson, S. Building a plant cell wall at a glance. J. Cell Sci. 2018, 131, s207373. [Google Scholar] [CrossRef] [Green Version]
  30. Jarvis, M.C.; Briggs, S.P.H.; Knox, J.P. Intercellular adhesion and cell separation in plants. Plant Cell Environ. 2003, 26, 977–989. [Google Scholar] [CrossRef]
  31. Zhang, B.; Gao, Y.; Zhang, L.; Zhou, Y. The plant cell wall: Biosynthesis, construction, and functions. J. Integr. Plant Biol. 2021, 63, 251–272. [Google Scholar] [CrossRef]
  32. Yokoyama, R.; Shinohara, N.; Asaoka, R.; Narukawa, H.; Nishitani, K. The biosynthesis and function of polysaccharide components of the plant cell wall. In Plant Cell Wall Patterning and Cell Shape; John Wiley & Sons: Hoboken, NJ, USA, 2014; Volume 1, pp. 3–34. [Google Scholar]
  33. Zheng, X.; Yuan, Y.; Huang, B.; Hu, X.; Tang, Y.; Xu, X.; Wu, M.; Gong, Z.; Luo, Y.; Gong, M.; et al. Control of fruit softening and ascorbic acid accumulation by manipulation of SlIMP3 in tomato. Plant Biotechnol. J. 2022, 20, 1213–1225. [Google Scholar] [CrossRef] [PubMed]
  34. Liu, J.; Zhao, Y.; Xu, H.; Zhao, X.; Tan, Y.; Li, P.; Li, D.; Tao, Y.; Liu, D. Fruit softening correlates with enzymatic activities and compositional changes in fruit cell wall during growing in Lycium barbarum L. Int. J. Food Sci. Technol. 2021, 56, 3044–3054. [Google Scholar] [CrossRef]
  35. Posé, S.; Paniagua, C.; Matas, A.J.; Gunning, A.P.; Morris, V.J.; Quesada, M.A.; Mercado, J.A. A nanostructural view of the cell wall disassembly process during fruit ripening and postharvest storage by atomic force microscopy. Trends Food Sci. Technol. 2019, 87, 47–58. [Google Scholar] [CrossRef]
  36. Tucker, G.; Yin, X.; Zhang, A.; Wang, M.; Zhu, Q.; Liu, X.; Xie, X.; Chen, K.; Grierson, D. Ethylene† and fruit softening. Food Qual. Saf. 2017, 1, 253–267. [Google Scholar] [CrossRef]
  37. Zamil, M.S.; Geitmann, A. The middle lamella—More than a glue. Phys. Biol. 2017, 14, 15004. [Google Scholar] [CrossRef] [PubMed]
  38. Vicente, A.R.; Rodoni, L.M.; Salato, G.S.; Basanta, M.F.; Ponce, N.; Stortz, C.A.; Raffo, M.D.; Powell, A.; Bennett, A.B.; Labavitch, J.M. Role of "well known" proteins on cell wall degradation and softening. Acta Hortic. 2015, 1079, 61–69. [Google Scholar] [CrossRef]
  39. Broxterman, S.E.; Schols, H.A. Characterisation of pectin-xylan complexes in tomato primary plant cell walls. Carbohyd. Polym. 2018, 197, 269–276. [Google Scholar] [CrossRef]
  40. Dumville, J.C.; Fry, S.C. Solubilisation of tomato fruit pectins by ascorbate: A possible non-enzymic mechanism of fruit softening. Planta 2003, 217, 951–961. [Google Scholar] [CrossRef]
  41. Brummell, D.A.; Dal Cin, V.; Crisosto, C.H.; Labavitch, J.M. Cell wall metabolism during maturation, ripening and senescence of peach fruit. J. Exp. Bot. 2004, 55, 2029–2039. [Google Scholar] [CrossRef] [Green Version]
  42. Phyo, P.; Wang, T.; Xiao, C.; Anderson, C.T.; Hong, M. Effects of pectin molecular weight changes on the structure, dynamics, and polysaccharide interactions of primary cell walls of Arabidopsis thaliana: Insights from solid-state NMR. Biomacromolecules 2017, 18, 2937–2950. [Google Scholar] [CrossRef]
  43. Xue, C.; Guan, S.; Chen, J.; Wen, C.; Cai, J.; Chen, X. Genome wide identification and functional characterization of strawberry pectin methylesterases related to fruit softening. BMC Plant Biol. 2020, 20, 13. [Google Scholar] [CrossRef] [PubMed]
  44. Zheng, L.; Xu, Y.; Li, Q.; Zhu, B. Pectinolytic lyases: A comprehensive review of sources, category, property, structure, and catalytic mechanism of pectate lyases and pectin lyases. Bioresour. Bioprocess. 2021, 8, 79. [Google Scholar] [CrossRef]
  45. Yang, Y.; Yu, Y.; Liang, Y.; Anderson, C.T.; Cao, J. A profusion of molecular scissors for pectins: Classification, expression, and functions of plant polygalacturonases. Front. Plant Sci. 2018, 9, 1208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Wen, B.; Ström, A.; Tasker, A.; West, G.; Tucker, G.A. Effect of silencing the two major tomato fruit pectin methylesterase isoforms on cell wall pectin metabolism. Plant Biol. 2013, 15, 1025–1032. [Google Scholar] [CrossRef] [PubMed]
  47. Hou, Y.; Wu, F.; Zhao, Y.; Shi, L.; Zhu, X. Cloning and expression analysis of polygalacturonase and pectin methylesterase genes during softening in apricot (Prunus armeniaca L.) fruit. Sci. Hortic. 2019, 256, 108607. [Google Scholar] [CrossRef]
  48. Zhang, W.; Zhao, S.; Gu, S.; Cao, X.; Zhang, Y.; Niu, J.; Liu, L.; Li, A.; Jia, W.; Qi, B.; et al. FvWRKY48 binds to the pectate lyase FvPLA promoter to control fruit softening in Fragaria vesca. Plant Physiol. 2022, 189, 1037–1049. [Google Scholar] [CrossRef]
  49. Xu, Z.; Dai, J.; Kang, T.; Shah, K.; Li, Q.; Liu, K.; Xing, L.; Ma, J.; Zhang, D.; Zhao, C. PpePL1 and PpePL15 are the core members of the pectate lyase gene family involved in peach fruit ripening and softening. Front. Plant Sci. 2022, 13, 844055. [Google Scholar] [CrossRef]
  50. Li, W.; Xu, L.; Xia, R.; Shen, Y.; Zhu, Z.; Yu, Y.; Zang, Y. Cloning and functional identification of SlPG49 in Solanum lycopersicum. Appl. Sci. 2021, 11, 11450. [Google Scholar] [CrossRef]
  51. Posé, S.; Paniagua, C.; Cifuentes, M.; Blanco-Portales, R.; Quesada, M.A.; Mercado, J.A. Insights into the effects of polygalacturonase FaPG1 gene silencing on pectin matrix disassembly, enhanced tissue integrity, and firmness in ripe strawberry fruits. J. Exp. Bot. 2013, 64, 3803–3815. [Google Scholar] [CrossRef]
  52. Qian, M.; Xu, Z.; Zhang, Z.; Li, Q.; Yan, X.; Liu, H.; Han, M.; Li, F.; Zheng, J.; Zhang, D.; et al. The downregulation of PpPG21 and PpPG22 influences peach fruit texture and softening. Planta 2021, 254, 22. [Google Scholar] [CrossRef]
  53. Khan, N.; Fatima, F.; Haider, M.S.; Shazadee, H.; Liu, Z.; Zheng, T.; Fang, J. Genome-Wide identification and expression profiling of the polygalacturonase (PG) and pectin methylesterase (PME) genes in grapevine (Vitis vinifera L.). Int. J. Mol. Sci. 2019, 20, 3180. [Google Scholar] [CrossRef] [PubMed]
  54. Xiao, L.; Li, T.; Jiang, G.; Jiang, Y.; Duan, X. Cell wall proteome analysis of banana fruit softening using iTRAQ technology. J. Proteom. 2019, 209, 103506. [Google Scholar] [CrossRef]
  55. Smith, D.L.; Abbott, J.A.; Gross, K.C. Down-regulation of tomato β-galactosidase 4 results in decreased fruit softening. Plant Physiol. 2002, 129, 1755–1762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Paniagua, C.; Blanco-Portales, R.; Barceló-Muñoz, M.; García-Gago, J.A.; Waldron, K.W.; Quesada, M.A.; Muñoz-Blanco, J.; Mercado, J.A. Antisense down-regulation of the strawberry β-galactosidase gene FaβGal4 increases cell wall galactose levels and reduces fruit softening. J. Exp. Bot. 2016, 67, 619–631. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Guo, S.; Song, J.; Zhang, B.; Jiang, H.; Ma, R.; Yu, M. Genome-wide identification and expression analysis of beta-galactosidase family members during fruit softening of peach [Prunus persica (L.) Batsch]. Postharvest Biol. Technol. 2018, 136, 111–123. [Google Scholar] [CrossRef]
  58. Liu, H.; Qian, M.; Song, C.; Li, J.; Zhao, C.; Li, G.; Wang, A.; Han, M. Down-Regulation of PpBGAL10 and PpBGAL16 delays fruit softening in peach by reducing polygalacturonase and pectin methylesterase activity. Front. Plant Sci. 2018, 9, 1015. [Google Scholar] [CrossRef]
  59. Cosgrove, D.J. Growth of the plant cell wall. Nat. Rev. Mol. Cell Bio. 2005, 6, 850–861. [Google Scholar] [CrossRef]
  60. Ma, M.; Yuan, Y.; Cheng, C.; Zhang, Y.; Yang, S. The MdXTHB gene is involved in fruit softening in ‘Golden Del. Reinders’ (Malus pumila). J. Sci. Food Agric. 2021, 101, 564–572. [Google Scholar] [CrossRef]
  61. Witasari, L.D.; Huang, F.; Hoffmann, T.; Rozhon, W.; Fry, S.C.; Schwab, W. Higher expression of the strawberry xyloglucan endotransglucosylase/hydrolase genes FvXTH9 and FvXTH6 accelerates fruit ripening. Plant J. 2019, 100, 1237–1253. [Google Scholar] [CrossRef] [Green Version]
  62. Han, Y.; Ban, Q.; Hou, Y.; Meng, K.; Suo, J.; Rao, J. Isolation and characterization of two persimmon xyloglucan endotransglycosylase/Hydrolase (XTH) genes that have divergent functions in cell wall modification and fruit postharvest softening. Front. Plant Sci. 2016, 7, 624. [Google Scholar] [CrossRef] [Green Version]
  63. Miedes, E.; Herbers, K.; Sonnewald, U.; Lorences, E.P. Overexpression of a cell wall enzyme reduces xyloglucan depolymerization and softening of transgenic tomato fruits. J. Agric. Food Chem. 2010, 58, 5708–5713. [Google Scholar] [CrossRef] [PubMed]
  64. Cosgrove, D.J. Plant expansins: Diversity and interactions with plant cell walls. Curr. Opin. Plant Biol. 2015, 25, 162–172. [Google Scholar] [CrossRef] [Green Version]
  65. Lu, Y.; Liu, L.; Wang, X.; Han, Z.; Ouyang, B.; Zhang, J.; Li, H. Genome-wide identification and expression analysis of the expansin gene family in tomato. Mol. Genet. Genom. 2016, 291, 597–608. [Google Scholar] [CrossRef] [PubMed]
  66. Dong, C.; Zou, X.; Gao, Q. Genome-wide identification of expansin in Fragaria vesca and expression profiling analysis of the FvEXPs in different fruit development. Gene 2022, 814, 146162. [Google Scholar] [CrossRef]
  67. Sane, V.A.; Sane, A.P.; Nath, P. Multiple forms of α-expansin genes are expressed during banana fruit ripening and development. Postharvest Biol. Technol. 2007, 45, 184–192. [Google Scholar] [CrossRef]
  68. Brummell, D.A.; Howie, W.J.; Ma, C.; Dunsmuir, P. Postharvest fruit quality of transgenic tomatoes suppressed in expression of a ripening-related expansin. Postharvest Biol. Technol. 2002, 25, 209–220. [Google Scholar] [CrossRef]
  69. Powell, A.L.T.; Kalamaki, M.S.; Kurien, P.A.; Gurrieri, S.; Bennett, A.B. Simultaneous transgenic suppression of LePG and LeExp1 influences fruit texture and juice viscosity in a fresh market tomato variety. J. Agric. Food Chem. 2003, 51, 7450–7455. [Google Scholar] [CrossRef]
  70. Valenzuela-Riffo, F.; Morales-Quintana, L. Study of the structure and binding site features of FaEXPA2, an α-expansin protein involved in strawberry fruit softening. Comput. Biol. Chem. 2020, 87, 107279. [Google Scholar] [CrossRef]
  71. Valenzuela-Riffo, F.; Parra-Palma, C.; Ramos, P.; Morales-Quintana, L. Molecular and structural insights into FaEXPA5, an alpha-expansin protein related with cell wall disassembly during ripening of strawberry fruit. Plant Physiol. Biochem. 2020, 154, 581–589. [Google Scholar] [CrossRef]
  72. Zhang, H.; Wang, H.; Li, H.; Zhang, H.; Duan, C.; Qiu, X.; Wang, Z. Study on the difference of EXP and PsEXPA10 in ripening period of ‘jinmi’plum and ‘qingcui’plum. IOP Conf. Ser. Earth Environ. Sci. 2021, 792, 12036. [Google Scholar] [CrossRef]
  73. Wu, B.; Shen, F.; Chen, C.J.; Liu, L.; Wang, X.; Zheng, W.Y.; Deng, Y.; Wang, T.; Huang, Z.Y.; Xiao, C.; et al. Natural variations in a pectin acetylesterase gene, MdPAE10, contribute to prolonged apple fruit shelf life. Plant Genome 2021, 14, e20084. [Google Scholar] [CrossRef] [PubMed]
  74. Jara, K.; Castro, R.I.; Ramos, P.; Parra-Palma, C.; Valenzuela-Riffo, F.; Morales-Quintana, L. Molecular insights into FaEG1, a strawberry endoglucanase enzyme expressed during strawberry fruit ripening. Plants 2019, 8, 140. [Google Scholar] [CrossRef] [Green Version]
  75. Farinati, S.; Rasori, A.; Varotto, S.; Bonghi, C. Rosaceae fruit development, ripening and post-harvest: An epigenetic perspective. Front. Plant Sci. 2017, 8, 1247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Fenn, M.A.; Giovannoni, J.J. Phytohormones in fruit development and maturation. Plant J. 2021, 105, 446–458. [Google Scholar] [CrossRef] [PubMed]
  77. Mou, W.; Li, D.; Bu, J.; Jiang, Y.; Khan, Z.U.; Luo, Z.; Mao, L.; Ying, T. Comprehensive analysis of ABA effects on ethylene biosynthesis and signaling during tomato fruit ripening. PLoS ONE 2016, 11, e154072. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Zaharah, S.S.; Singh, Z.; Symons, G.M.; Reid, J.B. Mode of action of abscisic acid in triggering ethylene biosynthesis and softening during ripening in mango fruit. Postharvest Biol. Technol. 2013, 75, 37–44. [Google Scholar] [CrossRef]
  79. Diretto, G.; Frusciante, S.; Fabbri, C.; Schauer, N.; Busta, L.; Wang, Z.; Matas, A.J.; Fiore, A.; Rose, J.K.; Fernie, A.R.; et al. Manipulation of β-carotene levels in tomato fruits results in increased ABA content and extended shelf life. Plant Biotechnol. J. 2020, 18, 1185–1199. [Google Scholar] [CrossRef] [Green Version]
  80. Sun, L.; Sun, Y.; Zhang, M.; Wang, L.; Ren, J.; Cui, M.; Wang, Y.; Ji, K.; Li, P.; Li, Q.; et al. Suppression of 9-cis-Epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol. 2012, 158, 283–298. [Google Scholar] [CrossRef] [Green Version]
  81. Mattus-Araya, E.; Stappung, Y.; Herrera, R.; Moya-León, M.A. Molecular actors involved in the softening of fragaria chiloensis fruit accelerated by ABA treatment. J. Plant Growth Regul. 2022. [Google Scholar] [CrossRef]
  82. Kai, W.; Wang, J.; Liang, B.; Fu, Y.; Zheng, Y.; Zhang, W.; Li, Q.; Leng, P. PYL9 is involved in the regulation of ABA signaling during tomato fruit ripening. J. Exp. Bot. 2019, 70, 6305–6319. [Google Scholar] [CrossRef] [Green Version]
  83. Zhou, Q.; Zhang, F.; Ji, S.; Dai, H.; Zhou, X.; Wei, B.; Cheng, S.; Wang, A. Abscisic acid accelerates postharvest blueberry fruit softening by promoting cell wall metabolism. Sci. Hortic. 2021, 288, 110325. [Google Scholar] [CrossRef]
  84. Li, Q.; Chen, P.; Dai, S.; Sun, Y.; Yuan, B.; Kai, W.; Pei, Y.; He, S.; Liang, B.; Zhang, Y.; et al. PacCYP707A2 negatively regulates cherry fruit ripening while PacCYP707A1 mediates drought tolerance. J. Exp. Bot. 2015, 66, 3765–3774. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Shin, M.H.; Kwack, Y.; Kim, Y.; Kim, J.G. Fruit ripening and related gene expression in ‘Goldone’and ‘Jecy Gold’kiwifruit by exogenous ethylene application. Korean J. Hortic. Sci. Technol. 2019, 37, 54–64. [Google Scholar]
  86. Villarreal, N.M.; Bustamante, C.A.; Civello, P.M.; Martínez, G.A. Effect of ethylene and 1-MCP treatments on strawberry fruit ripening. J. Sci. Food Agric. 2010, 90, 683–689. [Google Scholar] [CrossRef]
  87. Fan, X.; Shu, C.; Zhao, K.; Wang, X.; Cao, J.; Jiang, W. Regulation of apricot ripening and softening process during shelf life by post-storage treatments of exogenous ethylene and 1-methylcyclopropene. Sci. Hortic. 2018, 232, 63–70. [Google Scholar] [CrossRef]
  88. Soares, C.G.; Do Prado, S.B.; Andrade, S.C.S.; Fabi, J.P. Systems biology applied to the study of papaya fruit ripening: The influence of ethylene on pulp softening. Cells 2021, 10, 2339. [Google Scholar] [CrossRef]
  89. Cao, H.; Chen, J.; Yue, M.; Xu, C.; Jian, W.; Liu, Y.; Song, B.; Gao, Y.; Cheng, Y.; Li, Z. Tomato transcriptional repressor MYB70 directly regulates ethylene-dependent fruit ripening. Plant J. 2020, 104, 1568–1581. [Google Scholar] [CrossRef]
  90. Tieman, D.M.; Taylor, M.G.; Ciardi, J.A.; Klee, H.J. The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proc. Natl. Acad. Sci. USA 2000, 97, 5663–5668. [Google Scholar] [CrossRef] [Green Version]
  91. Kevany, B.M.; Tieman, D.M.; Taylor, M.G.; Cin, V.D.; Klee, H.J. Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J. 2007, 51, 458–467. [Google Scholar] [CrossRef]
  92. Hayama, H.; Shimada, T.; Fujii, H.; Ito, A.; Kashimura, Y. Ethylene-regulation of fruit softening and softening-related genes in peach. J. Exp. Bot. 2006, 57, 4071–4077. [Google Scholar] [CrossRef]
  93. Hu, Z.L.; Deng, L.; Chen, X.Q.; Wang, P.Q.; Chen, G.P. Co-suppression of the EIN2-homology gene LeEIN2 inhibits fruit ripening and reduces ethylene sensitivity in tomato. Russ. J. Plant Physiol. 2010, 57, 554–559. [Google Scholar] [CrossRef]
  94. Li, J.; Tao, X.; Li, L.; Mao, L.; Luo, Z.; Khan, Z.U.; Ying, T. Comprehensive RNA-Seq analysis on the regulation of tomato ripening by exogenous auxin. PLoS ONE 2016, 11, e156453. [Google Scholar] [CrossRef] [PubMed]
  95. Catalá, C.; Rose, J.K.; Bennett, A.B. Auxin-regulated genes encoding cell wall-modifying proteins are expressed during early tomato fruit growth. Plant Physiol. 2000, 122, 527–534. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Pan, L.; Zeng, W.; Niu, L.; Lu, Z.; Liu, H.; Cui, G.; Zhu, Y.; Chu, J.; Li, W.; Fang, W.; et al. PpYUC11, a strong candidate gene for the stony hard phenotype in peach (Prunus persica L. Batsch), participates in IAA biosynthesis during fruit ripening. J. Exp. Bot. 2015, 66, 7031–7044. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Wang, X.; Pan, L.; Wang, Y.; Meng, J.; Deng, L.; Niu, L.; Liu, H.; Ding, Y.; Yao, J.; Nieuwenhuizen, N.J.; et al. PpIAA1 and PpERF4 form a positive feedback loop to regulate peach fruit ripening by integrating auxin and ethylene signals. Plant Sci. 2021, 313, 111084. [Google Scholar] [CrossRef]
  98. Wang, J.; Su, W.; Liu, K.; Xu, Z.; Shah, K.; Ma, J.; Zhang, D.; Hu, Y.; Zhao, C. PpSAUR43, an auxin-responsive gene, is involved in the post-ripening and softening of peaches. Horticulturae 2022, 8, 379. [Google Scholar] [CrossRef]
  99. Gan, Z.; Fei, L.; Shan, N.; Fu, Y.; Chen, J. Identification and expression analysis of Gretchen Hagen 3 (GH3) in Kiwifruit (Actinidia chinensis) during postharvest process. Plants 2019, 8, 473. [Google Scholar] [CrossRef] [Green Version]
  100. Jia, H.; Xie, Z.; Wang, C.; Shangguan, L.; Qian, N.; Cui, M.; Liu, Z.; Zheng, T.; Wang, M.; Fang, J. Abscisic acid, sucrose, and auxin coordinately regulate berry ripening process of the Fujiminori grape. Funct. Integr. Genom. 2017, 17, 441–457. [Google Scholar] [CrossRef]
  101. Chen, J.; Mao, L.; Lu, W.; Ying, T.; Luo, Z. Transcriptome profiling of postharvest strawberry fruit in response to exogenous auxin and abscisic acid. Planta 2016, 243, 183–197. [Google Scholar] [CrossRef]
  102. Nolan, T.M.; Vukašinović, N.; Liu, D.; Russinova, E.; Yin, Y. Brassinosteroids: Multidimensional regulators of plant growth, development, and stress responses. Plant Cell 2020, 32, 295–318. [Google Scholar] [CrossRef] [Green Version]
  103. He, Y.; Li, J.; Ban, Q.; Han, S.; Rao, J. Role of brassinosteroids in persimmon (Diospyros kaki L.) fruit ripening. J. Agric. Food Chem. 2018, 66, 2637–2644. [Google Scholar] [CrossRef] [PubMed]
  104. Guo, Y.F.; Shan, W.; Liang, S.M.; Wu, C.J.; Wei, W.; Chen, J.Y.; Lu, W.J.; Kuang, J.F. MaBZR1/2 act as transcriptional repressors of ethylene biosynthetic genes in banana fruit. Physiol. Plant. 2019, 165, 555–568. [Google Scholar] [CrossRef] [PubMed]
  105. Zhu, T.; Tan, W.R.; Deng, X.G.; Zheng, T.; Lin, H.H. Effects of brassinosteroids on quality attributes and ethylene synthesis in postharvest tomato fruit. Postharvest Biol. Technol. 2015, 100, 196–204. [Google Scholar] [CrossRef]
  106. Hu, S.; Liu, L.; Li, S.; Shao, Z.; Meng, F.; Liu, H.; Duan, W.; Liang, D.; Zhu, C.; Xu, T.; et al. Regulation of fruit ripening by the brassinosteroid biosynthetic gene SlCYP90B3 via an ethylene-dependent pathway in tomato. Hortic. Res. 2020, 7, 163. [Google Scholar] [CrossRef]
  107. He, Y.; Liu, H.; Li, H.; Jin, M.; Wang, X.; Yin, X.; Zhu, Q.; Rao, J. Transcription factors DkBZR1/2 regulate cell wall degradation genes and ethylene biosynthesis genes during persimmon fruit ripening. J. Exp. Bot. 2021, 72, 6437–6446. [Google Scholar] [CrossRef] [PubMed]
  108. Han, Y.; Chen, C.; Yan, Z.; Li, J.; Wang, Y. The methyl jasmonate accelerates the strawberry fruits ripening process. Sci. Hortic. 2019, 249, 250–256. [Google Scholar] [CrossRef]
  109. Jia, H.; Zhang, C.; Pervaiz, T.; Zhao, P.; Liu, Z.; Wang, B.; Wang, C.; Zhang, L.; Fang, J.; Qian, J. Jasmonic acid involves in grape fruit ripening and resistant against Botrytis cinerea. Funct. Integr. Genom. 2016, 16, 79–94. [Google Scholar] [CrossRef]
  110. Kumar, N.; Tokas, J.; Raghavendra, M.; Singal, H.R. Impact of exogenous salicylic acid treatment on the cell wall metabolism and ripening process in postharvest tomato fruit stored at ambient temperature. Int. J. Food Sci. Technol. 2021, 56, 2961–2972. [Google Scholar] [CrossRef]
  111. Yin, W.; Hu, Z.; Cui, B.; Guo, X.; Hu, J.; Zhu, Z.; Chen, G. Suppression of the MADS-box gene SlMBP8 accelerates fruit ripening of tomato (Solanum lycopersicum). Plant Physiol. Biochem. 2017, 118, 235–244. [Google Scholar] [CrossRef]
  112. Li, S.; Chen, K.; Grierson, D. A critical evaluation of the role of ethylene and MADS transcription factors in the network controlling fleshy fruit ripening. New Phytol. 2019, 221, 1724–1741. [Google Scholar] [CrossRef] [Green Version]
  113. Shima, Y.; Fujisawa, M.; Kitagawa, M.; Nakano, T.; Kimbara, J.; Nakamura, N.; Shiina, T.; Sugiyama, J.; Nakamura, T.; Kasumi, T.; et al. Tomato FRUITFULL homologs regulate fruit ripening via ethylene biosynthesis. Biosci. Biotechnol. Biochem. 2014, 78, 231–237. [Google Scholar] [CrossRef] [Green Version]
  114. Elitzur, T.; Yakir, E.; Quansah, L.; Zhangjun, F.; Vrebalov, J.; Khayat, E.; Giovannoni, J.J.; Friedman, H. Banana MaMADS transcription factors are necessary for fruit ripening and molecular tools to promote Shelf-Life and food security. Plant Physiol. 2016, 171, 380–391. [Google Scholar] [CrossRef] [PubMed]
  115. Li, J.; Li, F.; Qian, M.; Han, M.; Liu, H.; Zhang, D.; Ma, J.; Zhao, C. Characteristics and regulatory pathway of the PrupeSEP1 SEPALLATA gene during ripening and softening in peach fruits. Plant Sci. 2017, 257, 63–73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Zhang, S.; Wang, X.; Xu, Z.; Shi, P.; Gu, M.; Kang, T.; Li, Q.; Zhang, D.; Zhao, C. PrupeFUL4 regulates ripening and softening of peach fruits through ethylene biosynthesis. Acta Physiol. Plant. 2022, 44, 23. [Google Scholar] [CrossRef]
  117. Qi, X.; Liu, C.; Song, L.; Li, M. PaMADS7, a MADS-box transcription factor, regulates sweet cherry fruit ripening and softening. Plant Sci. 2020, 301, 110634. [Google Scholar] [CrossRef]
  118. Gu, C.; Guo, Z.; Hao, P.; Wang, G.; Jin, Z.; Zhang, S. Multiple regulatory roles of AP2/ERF transcription factor in angiosperm. Bot. Stud. 2017, 58, 6. [Google Scholar] [CrossRef] [Green Version]
  119. Chung, M.; Vrebalov, J.; Alba, R.; Lee, J.; McQuinn, R.; Chung, J.; Klein, P.; Giovannoni, J. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 2010, 64, 936–947. [Google Scholar] [CrossRef]
  120. Liu, M.; Diretto, G.; Pirrello, J.; Roustan, J.; Li, Z.; Giuliano, G.; Regad, F.; Bouzayen, M. The chimeric repressor version of an Ethylene Response Factor (ERF) family member, Sl-ERF.B3, shows contrasting effects on tomato fruit ripening. New Phytol. 2014, 203, 206–218. [Google Scholar] [CrossRef] [Green Version]
  121. Deng, H.; Chen, Y.; Liu, Z.; Liu, Z.; Shu, P.; Wang, R.; Hao, Y.; Su, D.; Pirrello, J.; Liu, Y.; et al. SlERF.F12 modulates the transition to ripening in tomato fruit by recruiting the co-repressor TOPLESS and histone deacetylases to repress key ripening genes. Plant Cell 2022, 34, 1250–1272. [Google Scholar] [CrossRef]
  122. Cheng, C.; Liu, J.; Wang, X.; Wang, Y.; Yuan, Y.; Yang, S. PpERF/ABR1 functions as an activator to regulate PpPG expression resulting in fruit softening during storage in peach (Prunus persica). Postharvest Biol. Technol. 2022, 189, 111919. [Google Scholar] [CrossRef]
  123. Fu, C.; Han, Y.; Qi, X.; Shan, W.; Chen, J.; Lu, W.; Kuang, J. Papaya CpERF9 acts as a transcriptional repressor of cell-wall-modifying genes CpPME1/2 and CpPG5 involved in fruit ripening. Plant Cell Rep. 2016, 35, 2341–2352. [Google Scholar] [CrossRef] [PubMed]
  124. Han, Y.; Kuang, J.; Chen, J.; Liu, X.; Xiao, Y.; Fu, C.; Wang, J.; Wu, K.; Lu, W. Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol. 2016, 171, 1070–1084. [Google Scholar] [CrossRef] [PubMed]
  125. Yang, S.; Zhou, J.; Watkins, C.B.; Wu, C.; Feng, Y.; Zhao, X.; Xue, Z.; Kou, X. NAC transcription factors SNAC4 and SNAC9 synergistically regulate tomato fruit ripening by affecting expression of genes involved in ethylene and abscisic acid metabolism and signal transduction. Postharvest Biol. Technol. 2021, 178, 111555. [Google Scholar] [CrossRef]
  126. Gao, Y.; Wei, W.; Zhao, X.; Tan, X.; Fan, Z.; Zhang, Y.; Jing, Y.; Meng, L.; Zhu, B.; Zhu, H.; et al. A NAC transcription factor, NOR-like1, is a new positive regulator of tomato fruit ripening. Hortic. Res. 2018, 5, 75. [Google Scholar] [CrossRef] [Green Version]
  127. Gao, Y.; Wei, W.; Fan, Z.; Zhao, X.; Zhang, Y.; Jing, Y.; Zhu, B.; Zhu, H.; Shan, W.; Chen, J.; et al. Re-evaluation of the nor mutation and the role of the NAC-NOR transcription factor in tomato fruit ripening. J. Exp. Bot. 2020, 71, 3560–3574. [Google Scholar] [CrossRef]
  128. Ma, N.; Feng, H.; Meng, X.; Li, D.; Yang, D.; Wu, C.; Meng, Q. Overexpression of tomato SlNAC1transcription factor alters fruit pigmentation and softening. BMC Plant Biol. 2014, 14, 351. [Google Scholar] [CrossRef] [Green Version]
  129. Wang, J.; Tian, S.; Yu, Y.; Ren, Y.; Guo, S.; Zhang, J.; Li, M.; Zhang, H.; Gong, G.; Wang, M.; et al. Natural variation in the NAC transcription factor NONRIPENING contributes to melon fruit ripening. J. Integr. Plant Biol. 2022, 64, 1448–1461. [Google Scholar] [CrossRef]
  130. Shan, W.; Kuang, J.; Wei, W.; Fan, Z.; Deng, W.; Li, Z.; Bouzayen, M.; Pirrello, J.; Lu, W.; Chen, J. MaXB3 modulates MaNAC2, MaACS1, and MaACO1 stability to repress ethylene biosynthesis during banana fruit ripening. Plant Physiol. 2020, 184, 1153–1171. [Google Scholar] [CrossRef]
  131. Carrasco-Orellana, C.; Stappung, Y.; Mendez-Yañez, A.; Allan, A.C.; Espley, R.V.; Plunkett, B.J.; Moya-Leon, M.A.; Herrera, R. Characterization of a ripening-related transcription factor FcNAC1 from Fragaria chiloensis fruit. Sci. Rep. 2018, 8, 10524. [Google Scholar] [CrossRef] [Green Version]
  132. Martín-Pizarro, C.; Vallarino, J.G.; Osorio, S.; Meco, V.; Urrutia, M.; Pillet, J.; Casañal, A.; Merchante, C.; Amaya, I.; Willmitzer, L.; et al. The NAC transcription factor FaRIF controls fruit ripening in strawberry. Plant Cell 2021, 33, 1574–1593. [Google Scholar] [CrossRef]
  133. Tian, F.; Yang, D.; Meng, Y.; Jin, J.; Gao, G. PlantRegMap: Charting functional regulatory maps in plants. Nucleic Acids Res. 2020, 48, D1104–D1113. [Google Scholar] [CrossRef]
  134. Liu, M.; Zhang, Z.; Xu, Z.; Wang, L.; Chen, C.; Ren, Z. Overexpression of SlMYB75 enhances resistance to Botrytis cinerea and prolongs fruit storage life in tomato. Plant Cell Rep. 2021, 40, 43–58. [Google Scholar] [CrossRef] [PubMed]
  135. Cai, J.; Mo, X.; Wen, C.; Gao, Z.; Chen, X.; Xue, C. FvMYB79 positively regulates strawberry fruit softening via transcriptional activation of FvPME38. Int. J. Mol. Sci. 2021, 23, 101. [Google Scholar] [CrossRef] [PubMed]
  136. Shan, W.; Guo, Y.; Wei, W.; Chen, J.; Lu, W.; Yuan, D.; Su, X.; Kuang, J. Banana MaBZR1/2 associate with MaMPK14 to modulate cell wall modifying genes during fruit ripening. Plant Cell Rep. 2020, 39, 35–46. [Google Scholar] [CrossRef] [PubMed]
  137. Zhang, T.; Li, W.; Xie, R.; Xu, L.; Zhou, Y.; Li, H.; Yuan, C.; Zheng, X.; Xiao, L.; Liu, K. CpARF2 and CpEIL1 interact to mediate auxin–ethylene interaction and regulate fruit ripening in papaya. Plant J. 2020, 103, 1318–1337. [Google Scholar] [CrossRef] [PubMed]
  138. Liang, S.; Chen, S.; Liu, Z.; Shan, W.; Chen, J.; Lu, W.; Lakshmanan, P.; Kuang, J. MabZIP74 interacts with MaMAPK11-3 to regulate the transcription of MaACO1/4 during banana fruit ripening. Postharvest Biol. Technol. 2020, 169, 111293. [Google Scholar] [CrossRef]
  139. Song, C.; Shan, W.; Yang, Y.; Tan, X.; Fan, Z.; Chen, J.; Lu, W.; Kuang, J. Heterodimerization of MaTCP proteins modulates the transcription of MaXTH10/11 genes during banana fruit ripening. Biochim. Biophys. Acta Gene Regul. Mech. 2018, 1861, 613–622. [Google Scholar] [CrossRef]
  140. Li, Y.; Zhu, B.; Xu, W.; Zhu, H.; Chen, A.; Xie, Y.; Shao, Y.; Luo, Y. LeERF1 positively modulated ethylene triple response on etiolated seedling, plant development and fruit ripening and softening in tomato. Plant Cell Rep. 2007, 26, 1999–2008. [Google Scholar] [CrossRef]
  141. Teyssier, E.; Boureauv, L.; Chen, W.; Lui, R.; Degraeve-Guibault, C.; Stammitti, L.; Hong, Y.; Gallusci, P. 8—Epigenetic regulation during fleshy fruit development and ripening. In Applied Plant Genomics and Biotechnology; Poltronieri, P., Hong, Y., Eds.; Woodhead Publishing: Oxford, UK, 2015; pp. 133–151. [Google Scholar]
  142. Tang, D.; Gallusci, P.; Lang, Z. Fruit development and epigenetic modifications. New Phytol. 2020, 228, 839–844. [Google Scholar] [CrossRef] [PubMed]
  143. Hadfield, K.A.; Dandekar, A.M.; Romani, R.J. Demethylation of ripening specific genes in tomato fruit. Plant Sci. 1993, 92, 13–18. [Google Scholar] [CrossRef]
  144. Manning, K.; Tör, M.; Poole, M.; Hong, Y.; Thompson, A.J.; King, G.J.; Giovannoni, J.J.; Seymour, G.B. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 2006, 38, 948–952. [Google Scholar] [CrossRef] [PubMed]
  145. Zhong, S.; Fei, Z.; Chen, Y.; Zheng, Y.; Huang, M.; Vrebalov, J.; McQuinn, R.; Gapper, N.; Liu, B.; Xiang, J. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 2013, 31, 154–159. [Google Scholar] [CrossRef] [PubMed]
  146. Liu, R.; How-Kit, A.; Stammitti, L.; Teyssier, E.; Rolin, D.; Mortain-Bertrand, A.; Halle, S.; Liu, M.; Kong, J.; Wu, C.; et al. A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc. Natl. Acad. Sci. USA 2015, 112, 10804–10809. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  147. Lang, Z.; Wang, Y.; Tang, K.; Tang, D.; Datsenka, T.; Cheng, J.; Zhang, Y.; Handa, A.K.; Zhu, J. Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc. Natl. Acad. Sci. USA 2017, 114, E4511–E4519. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  148. Zhou, L.; Tian, S.; Qin, G. RNA methylomes reveal the m6A-mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening. Genome Biol. 2019, 20, 156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  149. Li, Z.; Pi, Y.; Fan, J.; Yang, X.; Zhai, C.; Chen, H.; Wang, F.; Ding, J.; Gu, T.; Li, Y.; et al. High mobility group A3 enhances transcription of the DNA demethylase gene SlDML2 to promote tomato fruit ripening. Plant Physiol. 2022, 189, 315–328. [Google Scholar] [CrossRef]
  150. Li, Z.; Jiang, G.; Liu, X.; Ding, X.; Zhang, D.; Wang, X.; Zhou, Y.; Yan, H.; Li, T.; Wu, K.; et al. Histone demethylase SlJMJ6 promotes fruit ripening by removing H3K27 methylation of ripening-related genes in tomato. New Phytol. 2020, 227, 1138–1156. [Google Scholar] [CrossRef]
  151. Zhao, L.; Lu, J.; Zhang, J.; Wu, P.; Yang, S.; Wu, K. Identification and characterization of histone deacetylases in tomato (Solanum lycopersicum). Front. Plant Sci. 2015, 5, 760. [Google Scholar] [CrossRef] [Green Version]
  152. Guo, J.; Hu, Z.; Yu, X.; Li, A.; Li, F.; Wang, Y.; Tian, S.; Chen, G. A histone deacetylase gene, SlHDA3, acts as a negative regulator of fruit ripening and carotenoid accumulation. Plant Cell Rep. 2018, 37, 125–135. [Google Scholar] [CrossRef] [PubMed]
  153. Guo, J.; Hu, Z.; Li, F.; Zhang, L.; Yu, X.; Tang, B.; Chen, G. Silencing of histone deacetylase SlHDT3 delays fruit ripening and suppresses carotenoid accumulation in tomato. Plant Sci. 2017, 265, 29–38. [Google Scholar] [CrossRef] [PubMed]
  154. Boureau, L.; How-Kit, A.; Teyssier, E.; Drevensek, S.; Rainieri, M.; Joubès, J.; Stammitti, L.; Pribat, A.; Bowler, C.; Hong, Y.; et al. A CURLY LEAF homologue controls both vegetative and reproductive development of tomato plants. Plant Mol. Biol. 2016, 90, 485–501. [Google Scholar] [CrossRef]
  155. Förderer, A.; Zhou, Y.; Turck, F. The age of multiplexity: Recruitment and interactions of Polycomb complexes in plants. Curr. Opin. Plant Biol. 2016, 29, 169–178. [Google Scholar] [CrossRef] [PubMed]
  156. Cheng, J.; Niu, Q.; Zhang, B.; Chen, K.; Yang, R.; Zhu, J.; Zhang, Y.; Lang, Z. Downregulation of RdDM during strawberry fruit ripening. Genome Biol. 2018, 19, 212. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  157. Hu, Y.; Han, Z.; Wang, T.; Li, H.; Li, Q.; Wang, S.; Tian, J.; Wang, Y.; Zhang, X.; Xu, X.; et al. Ethylene response factor MdERF4 and histone deacetylase MdHDA19 suppress apple fruit ripening through histone deacetylation of ripening-related genes. Plant Physiol. 2022, 188, 2166–2181. [Google Scholar] [CrossRef] [PubMed]
  158. Kuang, J.; Chen, J.; Luo, M.; Wu, K.; Sun, W.; Jiang, Y.; Lu, W. Histone deacetylase HD2 interacts with ERF1 and is involved in longan fruit senescence. J. Exp. Bot. 2012, 63, 441–454. [Google Scholar] [CrossRef] [PubMed]
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Figure 2. Regulation of ripening and softening of fleshy fruits by phytohormones (see text). It mainly consists of five aspects, including ETH, ABA, IAA, BR and other phytohormones, which are represented by different colors. Arrows indicate activation, while arrows with blunt-ends indicate inhibition, a line means that uncertainty is active or suppressed.
Figure 2. Regulation of ripening and softening of fleshy fruits by phytohormones (see text). It mainly consists of five aspects, including ETH, ABA, IAA, BR and other phytohormones, which are represented by different colors. Arrows indicate activation, while arrows with blunt-ends indicate inhibition, a line means that uncertainty is active or suppressed.
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Figure 3. Role of epigenetic modifications in ripening and softening of fleshy fruits. The arrows indicate activation, whereas arrows with blunt ends indicate inhibition (see text).
Figure 3. Role of epigenetic modifications in ripening and softening of fleshy fruits. The arrows indicate activation, whereas arrows with blunt ends indicate inhibition (see text).
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Table
Table 1. Regulation of cell wall metabolizing enzyme-related genes on the ripening and softening of fleshy fruits.
Table 1. Regulation of cell wall metabolizing enzyme-related genes on the ripening and softening of fleshy fruits.
Cell Wall Degrading EnzymeFunctionSpeciesEncoding GenesReference(s)
PME (EC 3.1.1.11)Removal of methyl groups from esterified pectinTomato (Solanum lycopersicum L.)PMEU1, PE1/2[43,46,47]
Apricot (Prunus armeniaca L.)PaPME1
Strawberry (Fragaria vesca L.)FvPME38, FvPME 39
PL (EC 4.2.2.2)Eliminative cleavage of pectate, yielding oligosaccharides with 4-deoxy-α-D-mann-4-enuronosyl groups at their nonreducing endsTomato (Solanum lycopersicum L.)PL[7,48,49]
Strawberry (Fragaria vesca L.)FvPLA
Peach (Prunus persica
(L.) Batsch)		PpePL1, PpePL15
PG (EC 3.2.1.15)Hydrolytic cleavage of α-l,4-galactouronosyl linkages in unesterified pectinTomato (Solanum lycopersicum L.)SlPG49[50,51,52,53]
Strawberry (Fragaria×ananassa Duch.)FaPG1
Peach (Prunus persica (L.) Batsch)PpPG21, PpPG22
Grapevine (Vitis vinifera L.)VvPG1, VvPG2
Banana (Musa acuminata Colla)MaPG3, MaPG4
Pear (Pyrus communis L.)PcPGl, PcPG3
β-Gal (EC 3.2.1.23)Removal of galactosyl residues increased from pectinTomato (Solanum lycopersicum L.)TBG4[55,56,57,58]
Strawberry (Fragaria × ananassa Duch.)FaβGal4
Peach (Prunus persica (L.) Batsch)PpBGAL2, PpBGAL16, PpBGAL10
XTH (EC 2.4.1.207)Hydrolysis of xyloglucan or catalytic breakage of 1,4-β-D-glycosidic bond of xyloglucan and transfer of glycosyl groupsApple (Malus × domestica Borkh.)MdXTHB[60,61,62,63]
Strawberry (Fragaria vesca L.)FvXTH6, FvXTH9
Persimmon (Diospyros kaki Thunb.)DkXTH6, DkXTH7
Tomato (Solanum lycopersicum L.)SlXTH1
ExpansinWall stress relaxation and irreversible wall extensionTomato (Solanum lycopersicum L.)LeEXP1[67,69,70,71,72]
Plum (Prunus spp.)PsEXPA10
Strawberry (Fragaria × ananassa Duch.)FaEXPA2, FaEXPA5
Banana (Musa acuminata Colla)MaEXP1
Other enzymesPectin acetylesterase (PAE)Hydrolysis of acetyl esters of pectin, producing pectate, partially esterified pectinApple (Malus × domestica Borkh.)MdPAE10[73]
endo-1,4-β-D-glucanohydrolase (EC 3.2.1.4)Hydrolysis of soluble cellulose to produce reducing oligosaccharidesStrawberry (Fragaria × ananassa Duch.)FaEG1[74]
Table
Table 2. TFs involved in the regulation of ripening and softening in fleshy fruits.
Table 2. TFs involved in the regulation of ripening and softening in fleshy fruits.
TF TypesSpeciesTFs Related to Fruit Ripening and SofteningTarget GenesInteracting ProteinsReferences
MADS-boxTomato (Solanum lycopersicum L.)RINPG, TBG4, EXP1, CEL2, etc.FUL1/FUL2, TAGL1, SlMBP15, SlCMB1, NAC4, etc.[112,113]
SlMBP8/RIN[111]
Banana (Musa acuminata Colla)MaMADS1, MaMADS2//[114]
Peach (Prunus persica (L.) Batsch.)PrupeSEP1PrupePG2, PrupePG3/[115]
PrupeFUL4//[116]
Sweet cherry (Prunus avium L.)PaMADS7PaPG1/[117]
AP2/ERF Tomato (Solanum lycopersicum L.)AP2a//[119]
LeERF1 [140]
SlERF.B3//[120]
SlERF.F12ACS2, ACS4, PG2a, PLTPL2, SlDHA1, SlDHA3[121]
Banana (Musa acuminata Colla)MaERF11MaACO1, MaEXP2, MaEXP7, MaEXP8MaHDA1[124]
Peach (Prunus persica (L.) Batsch.)PpERF4PpNCED2, PpNCED3, PpPG1, PpACO1, PpIAA1PpIAA1[97]
PpERF/ABR1PpPG/[122]
Papaya (Carica papaya L.)CpERF9CpPME1/2, CpPG5/[123]
Apple (Malus × domestica Borkh.)MdERF4MdERF3MdTPL4[16]
NACTomato (Solanum lycopersicum L.)NOR-like1(SNAC4)SAPK3, SlCYP707A1, SlACO6, SlACS8, SlPG2a, SlPL, SlCEL2, SlEXP1SAPK3, SlPYL9, SlACS2, SlACO1[125,126]
NORSlACS2, SlGgpps2, SlPL/[127]
SlNAC1SlPSY1, SlACS2, SlACO1/[128]
Melon (Cucumis melo L.)CmNAC-NORCmACS5, CmNCED3/[129]
Banana (Musa acuminata L.)MaNAC1MaERF11, MaXB3/[130]
MaNAC2MaERF11, MaXB3MaXB3
Chilean strawberry (Fragaria chiloensis (L.) Duch.)FcNAC1FcPL/[131]
Strawberry (Fragaria × ananassa Duch.)FaRIF(FaNAC035)//[132]
MYBTomato (Solanum lycopersicum L.)SlMYB70SlACS2, SlACO3/[89]
SlMYB75SlFSR/[134]
Wild strawberry (Fragaria vesca L.)FvMYB79FvPME38/[135]
BZRTomato (Solanum lycopersicum L.)SlBES1PMEU1/[20]
Banana (Musa acuminata Colla)MaBZR1/2MaEXP2, MaPL2, MaXET5MaMPK14[136]
OthersGRASTomato (Solanum lycopersicum L.)SlFSR//[17]
ARFPapaya (Carica papaya L.)CpARF2/CpEIL1[137]
LOBTomato (Solanum lycopersicum L.)SlLOB1EXP1, CEL2, XY, AGP2, TBL, E6, PL/[15]
WRKYWild strawberry (Fragaria vesca L.)FvWRKY48FvPLA/[48]
bZIPBanana (Musa spp.)MabZIP74MaACO1/4MaMAPK11-3[138]
bHLHBanana (Musa spp.)MaTCP5, MaTCP19,MaXTH10/11MaTCP20[139]
MaTCP20MaXTH10/11MaTCP5, MaTCP19,
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Peng, Z.; Liu, G.; Li, H.; Wang, Y.; Gao, H.; Jemrić, T.; Fu, D. Molecular and Genetic Events Determining the Softening of Fleshy Fruits: A Comprehensive Review. Int. J. Mol. Sci. 2022, 23, 12482. https://doi.org/10.3390/ijms232012482

AMA Style

Peng Z, Liu G, Li H, Wang Y, Gao H, Jemrić T, Fu D. Molecular and Genetic Events Determining the Softening of Fleshy Fruits: A Comprehensive Review. International Journal of Molecular Sciences. 2022; 23(20):12482. https://doi.org/10.3390/ijms232012482

Chicago/Turabian Style

Peng, Zhenzhen, Gangshuai Liu, Hongli Li, Yunxiang Wang, Haiyan Gao, Tomislav Jemrić, and Daqi Fu. 2022. "Molecular and Genetic Events Determining the Softening of Fleshy Fruits: A Comprehensive Review" International Journal of Molecular Sciences 23, no. 20: 12482. https://doi.org/10.3390/ijms232012482

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