Advancements on the Mechanism of Soluble Sugar Metabolism in Fruits

Abstract

Soluble sugars, primarily fructose, glucose, sucrose, and sorbitol, are crucial determinants of fruit flavor and quality. As a core component of biological metabolism, sugar metabolism provides energy and carbon for fruit development, ultimately governing carbohydrate accumulation in mature fruits. This process requires the coordinated activities of multiple enzymes and transporters, modulated by the spatiotemporal expression patterns of their encoding genes. Therefore, it is essential to elucidate both the activities of these enzymes across different fruits and their underlying gene expression patterns. While significant progress has been made in functional genes involved in soluble sugar metabolism and deciphering their regulatory networks, an overall introduction of this knowledge remains lacking. This review presents an integrative analysis of soluble sugar accumulation during fruit development, encompassing spatiotemporal dynamics of key metabolic enzymes, functional characterization of encoding genes, signaling response mechanisms governing gene regulation, and the overarching genetic network.

1. Introduction

Sugar content is a critical parameter in fruit quality evaluation, serving as a key sensory attribute prioritized by consumers and the primary high-quality breeding target [1]. Fruit sweetness perception primarily reflects the composition and concentration of soluble sugars, predominantly sucrose, fructose, glucose, and sorbitol. Soluble sugar metabolism involves spatiotemporal coordination of enzymes, genes, and signaling pathways. Key enzymes regulate sugar synthesis, allocation, and accumulation. Therefore, elucidating their gene expression and activity across species is fundamental to improving fruit quality.

Over the past decade, research on soluble sugar metabolism in fruit has focused on the regulation of core enzymes and genes, sugar composition–quality relationships, environmental responses of metabolism, transport protein functions, transcriptional networks, and multi-omics metabolic mapping. Figure 1 presents a core-periphery architecture consisting of a core, intermediate layers, and peripheral layers. The core is densely interconnected and includes key concepts such as soluble sugar metabolism, gene expression, and fruit quality. It reflects the continuous scientific research on the mechanisms of sugar source–sink transport and accumulation. The intermediate layer is characterized by terms such as transcription factors, epigenetics, and transcriptional regulation, signifying a paradigm shift from single gene analysis to systematic research at the level of regulatory networks. The peripheral layer records the emergence of specific metabolic enzymes (e.g., SPS, SUS, FRK, S6PDH) and specialized terminology (e.g., gene families, genetic interactions), demonstrating advancements in sugar signaling pathways, stress response mechanisms, and fruit quality engineering. Notably, aspects such as nutritional components, sweetness, and fruit flavor, which appear as characteristic keywords, have significantly increased since 2020, underscoring the progressively tighter integration between basic research and practical applications for improving fruit quality (Figure 1). Analysis of fruit soluble sugar metabolism research trends over the past decade reveals distinct publication patterns. From 2014 to 2018, the number of research papers was relatively low and fluctuated minimally. Since 2019, it has shown a significant growth trend and reached its peak in 2024. Notably, 2022 was the year with the highest growth rate, indicating that this field has achieved a paradigm shift driven by the popularization of omics technologies and the demand for fruit quality (Figure 2).

With the scope expanding from physiological and biochemical studies to multi-dimensional omics integration, shifting from single enzymes to regulatory networks of enzymes, transporters, and transcription factors. This progress supports flavor and nutritional enhancement. While advances include physiological roles of enzymes in sugar allocation and accumulation and functional characterization of sugar-metabolizing enzyme genes, signal transduction mechanisms, and network-level interactions remain poorly understood. This review synthesizes: soluble sugar profiles, developmental accumulation patterns, enzyme spatiotemporal dynamics, key gene functions, and molecular mechanisms of signaling and genetic networks. The aim is to deepen mechanistic insights and establish a framework for optimizing fruit flavor and economic value.

2. Soluble Sugar Composition and Accumulation Patterns in Fruit

Fruit tissues predominantly accumulate fructose, glucose, and sucrose, with minor quantities of sugar alcohols (e.g., sorbitol, myo-inositol). Fructose exhibits the highest relative sweetness, being 1.73 times sweeter than sucrose and 2.34 times sweeter than glucose. Thus, perceived sweetness depends not only on total sugar content but also on sugar composition and molar ratios. Chen et al. classify fruits into three main categories based on sugar accumulation patterns and characteristics: starch conversion type, direct sugar accumulation type, and mixture type [1]. Except for the direct sugar-accumulating type, which is typically non-climacteric, the others are predominantly climacteric (

Table 1. Sugar accumulation in fruits.

Sugar Accumulation Pattern	Type	Representative Fruit	Forms of Sugar Accumulation
Starch conversion type	Climacteric	Mango Banana Kiwifruit	Starch accumulates during fruit growth, development, and maturation. Post—harvest, starch converts to soluble sugars via sugar metabolism—related enzymes during ripening.
Sugar direct accumulation type	Non-climacteric	Strawberry Citrus Lychee Longan Grape Pitaya	Upon entry into fruits, most photosynthates are stored as soluble sugars in vacuoles during early fruit growth, with only a small fraction used for starch accumulation.
Mixture type	Climacteric	Apple Pear Peach	Starch accumulates during early growth, while in later stages, either soluble sugars accumulate directly or starch converts to soluble sugars for storage.

).

2.1. Starch Conversion Type

In starch-converting species, photoassimilates synthesized in source leaves are transported via the phloem to the fruit. Aside from supporting growth, development, and respiratory metabolism, these compounds are primarily converted into and stored as starch. Post-harvest, starch is enzymatically hydrolyzed into soluble sugars, predominantly mediated by sugar-metabolizing enzymes. Most of these fruit trees are climacteric, including mango, banana, and kiwifruit. In mango, starch accumulation occurs primarily during early fruit development, with content gradually increasing to a peak around 120 days post-anthesis (coinciding with full bloom). During this phase, soluble sugars (glucose, fructose, and sucrose) remain low, with sucrose nearly undetectable [2]. As maturation progresses, accelerated starch degradation causes a significant decrease in starch content, while sucrose levels rise rapidly. Glucose and fructose concentrations also increase, with fructose peaking during late maturity [3]. In kiwifruit, starch metabolism follows a dynamic pattern: content is initially low, increases during growth, peaks pre-harvest, and then degrades rapidly into soluble sugars during post-harvest storage [4]. In banana, early development features progressive starch accumulation until just before ripening. Soluble sugars remain low, with sucrose nearly undetectable. Upon ripening, the enzymatic breakdown of starch into soluble sugars enhances fruit sweetness. This process involves a sharp decline in starch content and a rapid rise in sucrose, glucose, and fructose concentrations [5].

2.2. Sugar Direct Accumulation Type

This category primarily stores soluble sugars in vacuoles early in development following photosynthate import, with minimal starch accumulation. They are predominantly non-climacteric, exhibiting stable respiration and ethylene emission rates throughout ripening. Examples include strawberry, citrus, lychee, longan, grape, and pitaya. Sucrose-accumulating fruits exhibit limited starch biosynthetic capacity; consequently, sucrose accumulation during development primarily results from translocation from source leaves. Within fruit cells, the sucrose synthesis capacity is relatively weak in early stages. However, sucrose phosphate synthase (SPS) activity significantly increases during ripening, synergistically enhanced by cell wall degradation, which facilitates sucrose biosynthesis.

2.2.1. The Accumulation Pattern of Soluble Sugars in Strawberry

In strawberry, glucose and fructose levels gradually increase during development, whereas sucrose levels surge markedly later [6]. Studies indicate that ripening involves a doubling of glucose and fructose concentrations, while sucrose increases by about 25-fold [7].

2.2.2. The Accumulation Pattern of Soluble Sugars in Citrus

In citrus, glucose, fructose, and sucrose constitute the primary soluble sugars. Early development features low sugar content, primarily composed of fructose and glucose. In sucrose-accumulating varieties, sucrose concentration rises steadily during cell expansion, exhibits a slower accumulation rate during the color-change phase, and peaks at maturity, while glucose and fructose increase gradually [8]. In hexose-accumulating fruits, sucrose and fructose levels are high from cell division to expansion. Fructose and glucose increase sharply during late expansion, peaking at maturity, while sucrose declines to its lowest point [9].

2.2.3. The Accumulation Pattern of Soluble Sugars in Lychee

In lychee, total soluble sugar content gradually increases during ripening. However, studies by Huang et al. on the ‘Guiwei’ cultivar indicate that, due to the dilution effect caused by fruit expansion and water influx, the total sugar content may decline before rapid accumulation [10]. Sugar component dynamics vary by cultivars. In ‘Nuomici’, sucrose rises, declines, then rises again, while glucose and fructose increase continuously; in cultivars like ‘Feizixiao’, ‘Huaizhi’, and ‘Guiwei’, glucose and fructose gradually increase, whereas sucrose rises then declines [11,12]. Pericarp reducing sugars typically increase rapidly late in development. However, some cultivars (e.g., ‘Feizixiao’, predominantly accumulating reducing sugars) undergo a “de-sugar” phase near full maturity [13].

2.2.4. The Accumulation Pattern of Soluble Sugars in Longan

In longan, sugar accumulation occurs in two primary phases: the initial accumulation phase and the subsequent “de-sugar” phase. The pericarp and aril contain sucrose, glucose, and fructose, with sucrose predominant at maturity, followed by glucose, and then fructose [14]. The “de-sugar” phenomenon near full maturity may relate to differential expression of genes involved in the glycolytic pathway. These genes are highly expressed at the onset of ripening and maintain elevated levels throughout both sugar accumulation and degradation phases.

2.2.5. The Accumulation Pattern of Soluble Sugars in Grape

In grape, glucose and fructose are predominant, with trace sucrose. During fruit enlargement, glucose and fructose rapidly accumulate and remain stable through to harvest. Sucrose, the main phloem-transported sugar early in development, is hydrolyzed during growth to produce glucose and fructose, resulting in negligible sucrose levels in mature fruits [15].

2.2.6. The Accumulation Pattern of Soluble Sugars in Pitaya

In pitaya, primary sugars are fructose, glucose, and trace sucrose. Immature fruit accumulates sucrose extensively, with relatively low fructose and glucose. From the immature to the color change stage, glucose and fructose begin to accumulate significantly. Between color change and full maturity, sugar content continues to increase, with glucose and fructose rising gradually, whereas sucrose decreases due to hydrolysis during ripening [16].

2.3. Mixture Type

The mixture type refers to the situation where photosynthates are introduced into the fruit during the early and middle stages of fruit development. After entering the fruit, they are converted into starch and accumulate within the fruit. In later stages, photosynthates are directly imported as soluble sugars, while stored starch undergoes hydrolysis, collectively driving sugar accumulation. This category encompasses predominantly climacteric rosaceae fruits (e.g., apple, pear, and peach). In apple, fructose is the predominant soluble sugar, followed by sucrose and glucose, with minimal sorbitol [17]. In peach, glucose and fructose prevail initially, but sucrose rapidly accumulates during maturation, accounting for 40% to 85% of total sugars [18]. Although proportions vary by cultivar and region, fructose and glucose typically accumulate to comparable levels [19]. In pear, sucrose is nearly absent until pre-ripening, only accumulating briefly before maturity. Sugar content increases progressively with fruit enlargement, showing a significant rise during ripening. At maturity, sucrose is the primary soluble sugar, with glucose and fructose present at lower concentrations [20].

3. Spatiotemporal Distribution of Enzymes Involved in Soluble Sugar Metabolism in Fruits

Ultimately, sucrose, fructose, and glucose are distributed across various fruit tissues, defining flavor profiles (Figure 3). Fruit carbohydrate metabolism involves three main pathways: sucrose metabolism, hexose metabolism, and sorbitol metabolism. Regulation of soluble sugar metabolism is highly complex, involving multiple metabolic enzymes and dynamic shifts in soluble sugar content and enzyme activity across different developmental stages, which play a decisive role in deciphering fruit carbohydrate metabolism.

3.1. Sucrose Metabolism

Sucrose, the primary end product of photosynthesis in higher plants, plays a central role in physiological processes including plant growth, fruit quality, and stress response. Beyond fueling cellular vitality and proliferation, it functions as a signaling molecule that modulates fruit development through sugar signaling pathways [21]. Key enzymes involved in sucrose metabolism include sucrose-phosphate synthase (SPS), sucrose synthase (SUS), and invertase (INV). Synthesized in source leaves, sucrose is transported to sink organs for storage or hydrolyzed by invertase into glucose and fructose in tissues requiring energy or carbon sources. SPS catalyzes sucrose biosynthesis. SUS, a glycosyl transferase, reversibly cleaves sucrose into uridine diphosphate glucose (UDPG) and fructose. In sink tissues, SUS predominantly facilitates the degradation of sucrose to supply hexoses for biosynthesis and respiration [22], with its reversibility being pH-dependent [23]. INV irreversibly hydrolyzes sucrose into glucose and fructose, serving as an essential energy source and signaling molecule in plant growth, stress response, carbohydrate allocation, and source–sink regulation [24]. Based on subcellular localization and optimal pH, invertases are classified into three subtypes: cell wall invertase (CWIN), vacuolar invertase (VIN), and cytoplasmic invertase (CIN). CWIN and VIN belong to the β-fructofuranosidase family, catalyzing the hydrolysis of the terminal non-reducing β-fructofuranosyl residues of sucrose to cleave sucrose into hexoses [25]. CIN, a newly identified member of the glycoside hydrolase family, specifically hydrolyzes sucrose into glucose and fructose [26]. CWIN, a non-plastidic acid invertase (AI), is tightly associated with the cell wall. It facilitates sucrose unloading by hydrolyzing apoplastic sucrose, thereby enhancing the sucrose concentration gradient from source to sink and participating in sucrose partitioning, osmotic regulation, stress response, and signal transduction [27,28]. VIN and CIN are plastidial invertases: VIN functions as an AI within vacuoles, regulating hexose and sucrose levels to influence cell expansion and sugar accumulation [29]. CIN, a neutral or alkaline invertase (NI), localizes to the cytoplasm and organelles (e.g., mitochondria and plastids) and exhibits substrate specificity for the α-1,2-glycosidic bond of sucrose [30].

During the pre-maturation phase of ‘KRS’ mango development, SPS activity peaks at 60 days post-anthesis, followed by a progressive decline until 120 days, hitting its lowest at 100 days. In the late stage, SPS activity stabilizes, peaking at full ripeness. SUS activity remains stable from 40 to 110 days post-anthesis, reaching its maximum at maturity. Meanwhile, AI activity rises throughout development, while NI activity stays relatively constant (Figure 4A), correlating with fruit sucrose accumulation [31].

Studies on ‘Tainong No. 1’ mango demonstrated that SPS activity increases slowly from 0 to 60 days, then rapidly until peaking at 90 days, with a slight decline at full ripeness. SUS activity slightly decreases during 0–15 days but then increases gradually to its maximum at maturity. AI activity surges rapidly in the first 15 days, stabilizes between 15 and 60 days, and then increases sharply to peak at 90 days before declining slightly at ripeness (Figure 4B). These trends significantly correlate with soluble sugar content, consistent with Wu’s findings [32].

During ‘Shixia’ longan development, NI activity decreases from a high baseline, while AI activity remains low, exhibiting a decline–rise–decline pattern. Sucrose synthase (cleavage direction) activity increases rapidly to an early peak (3.8-fold higher than the initial level), followed by a sharp decline. A slight rebound occurs at 65 days post-anthesis before gradually stabilizing by 75 days. The pericarp of longan exhibits a pattern of SPS activity rising initially, then declining, with a slow decrease after 65 days post-anthesis (Figure 4C). Analysis of soluble sugars in longan pericarp indicates that fructose and glucose are the primary accumulated sugars, predominantly regulated by NI and SUS. In contrast, sucrose accumulation occurs mainly in the pulp, with AI and SUS playing key enzymatic roles. This suggests differential activity and physiological functions of sucrose metabolism enzymes across developmental stages and tissue types [33].

Sugar content and related enzyme activity during ‘Hetao’ honeydew melon expansion, revealing that SUS (synthesis direction) maintains high activity across source-to-sink pathways, with tissue-specific variation. SUS activity is lowest in source leaves and highest in conducting tissues, while SPS activity remains very low across all tissues. Pulp invertase activity peaks significantly above other tissues, with NI activity consistently low and AI activity markedly exceeding NI. Sucrose content displays a decreasing gradient from leaves and conducting tissues to pulp, with fructose and glucose levels highest in pulp. The combined action of SUS, SPS, and INV facilitates sucrose synthesis in source leaves and degradation in sink fruits, establishing a concentration gradient [34].

Recent studies indicate that different rootstocks influence sugar accumulation and sucrose-metabolizing enzymes in watermelon. Liu et al. compared ‘Meidu’ watermelon grafted onto wild watermelon rootstock (WGW), pumpkin rootstock (PGW), and self-rooted ‘Meidu’ (SRW). It revealed that during fruit development, SUS, SPS, AI, and NI activities remain relatively stable with an initial increase followed by a decrease, with SPS activity highest in WGW. In contrast, INV activity is higher in PGW and SRW, while SUS synthesis activity remains low throughout development. The wild watermelon rootstock enhances sucrose synthesis by increasing SPS activity and suppressing invertase activity, thereby increasing total sugar content. Conversely, pumpkin rootstock’s high invertase activity promotes soluble sugar hydrolysis, reducing total sugar accumulation [35].

3.2. Sorbitol Metabolism

Sorbitol is a signature photosynthetic product and translocated carbohydrate in woody rosaceae fruit trees, accounting for 60–80% of photoassimilates [36]. Key enzymes involved in sorbitol metabolism comprise: sorbitol-6-phosphate dehydrogenase (S6PDH), which catalyzes sorbitol synthesis; NAD⁺-dependent sorbitol dehydrogenase (NAD⁺-SDH), responsible for sorbitol catabolism via oxidation to fructose; NADP⁺-dependent sorbitol dehydrogenase (NADP⁺-SDH), involved in sorbitol breakdown; and sorbitol oxidase (SOX), which oxidizes sorbitol to glucose. S6PDH is predominantly localized in leaf tissues, facilitating sorbitol biosynthesis, whereas SDH enzymes are primarily found in fruit and young leaf tissues, catalyzing sorbitol degradation. SOX activity is negligible in mature leaves but prominent in fruit and juvenile tissues.

In the ‘Korla Fragrant’ pear, sorbitol dominates soluble sugars (>50%) during early development but declines to ~24.7% at maturity. Both NAD⁺-SDH and SOX activities exhibit biphasic dynamics: decreasing initially during cell division and then increasing through ripening, with NAD⁺-SDH consistently exceeding SOX activity in magnitude and fluctuation amplitude. Critically, SDH activity correlates negatively with both sorbitol and total soluble sugar content, while SOX correlates negatively only with sorbitol [37]. Wang et al. investigated the differences in sugar accumulation and associated enzyme activities among various pear cultivars. Results demonstrated that at fruit maturity, the highest fructose contents were observed in ‘Yali’, ‘Chili’, and ‘Balixiang’, constituting 43.35%, 57.61%, and 38.95% of total sugars, respectively, with glucose levels being secondary and sucrose consistently the lowest. Variations in glucose and fructose contents were primarily influenced by NAD⁺-SDH and NADP⁺-SDH activities. NAD⁺-SDH activity, while temporally consistent across cultivars, is persistently highest in ‘Chili’, whereas NADP⁺-SDH activity remains elevated in ‘Yali’ [38].

Yang et al., using ‘Jinguan’ apple and its yield-superior line (SGP-1), found that SDH activity peaks unimodally at 127 days post-anthesis (DPA) in ‘Jinguan’ versus 47 DPA in its superior line ‘SGP-1’. During fruit growth, SOX activity in both cultivars showed opposite trends between 7 and 87 days post-anthesis: ‘Jinguan’ decreased then increased, whereas ‘SGP-1’ increased then decreased. From 107 to 167 days post-anthesis, SOX activity trends converged, both exhibiting a decline followed by an increase. Correlation analysis indicated that sorbitol content in both fruits exhibited a significant negative correlation with SDH activity during early development stages, while demonstrating a pronounced positive correlation in later stages. This pattern indicates a primary role of SDH in sugar accumulation during early development [39]. In loquat, Wu et al. observed decreasing sorbitol content throughout development, with ‘Baili’ maintaining higher levels than ‘Jiefangzhong’. Additionally, SDH and SOX activities showed an initial decline followed by a subsequent increase. However, significant differences in sorbitol content and enzyme activities were observed among cultivars during the expansion phase, potentially contributing to their quality differences [40].

3.3. Hexose Metabolism

Sucrose is hydrolyzed into glucose and fructose by INV or SUS. Both glucose and fructose are phosphorylated to form glucose-6-phosphate (G6P) and fructose-6-phosphate (F6P), respectively, before entering glycolytic or starch biosynthesis pathways [41]. Hexokinase (HXK) and fructokinase (FRK) catalyze hexose phosphorylation, mediating the initial irreversible step of hexose metabolism. These enzymes serve as critical regulatory points in plant energy metabolism and biosynthetic processes [42]. FRK, localized in plastids or the cytosol, specifically phosphorylates fructose to produce F6P. It has a substrate affinity two orders of magnitude higher than HXK, making it key to fructose phosphorylation and catabolism. Additionally, FRK activity is essential for cellulose biosynthesis and vascular development [43]. Most FRKs are substrate-dependent; high fructose concentrations inhibit activity, reducing F6P formation and limiting fructose flux through cytosolic glycolysis. This promotes fructose utilization in plastidial pathways like oxidative phosphorylation, pentose phosphate pathway, starch synthesis, and oxalate metabolism [44]. In dicotyledonous plants, HXK localizes to mitochondria or plastids, catalyzing the phosphorylation of glucose and fructose derived from sucrose hydrolysis, starch degradation, and polyol breakdown (e.g., mannitol, sorbitol, and galactose) from raffinose family oligosaccharides. Glucose serves as the preferred substrate [45]. Glucose-6-phosphate facilitates glycolysis and is a precursor for the pentose phosphate pathway, supporting biosynthesis of starch, cell wall polysaccharides, and fatty acids [42].

N-acetyl-D-glucosamine (NAG) treatment significantly inhibits HXK activity during postharvest kiwi fruit ripening. During storage, HXK activity increases and then decreases, but NAG-treated kiwi fruit consistently exhibits lower HXK activity than controls, with significant differences after two days [46]. Research by Shuai et al. demonstrated that in ‘Shixia’ longan fruit development, pericarp FRK activity declines with maturation, reaching its lowest at 101 days post-anthesis and then increasing significantly at 110 days. The correlation between changes in sugar content and FRK activity indicates that rapid sugar accumulation coincides with suppressed activity of FRK and its homologs. However, increased fructokinase activity during later ripening stages is associated with enhanced respiratory metabolism, providing energy for maturation and senescence [47].

4. Key Enzymatic Gene Response Signaling Pathways and Genetic Regulatory Networks

Fruit sweetness, as a quantitative trait, is not solely regulated by a single gene encoding key enzymes involved in soluble sugar metabolism. Instead, it is finely modulated by multiple signaling pathways. Exogenous environmental cues and endogenous hormonal signals regulate transcription and translation of critical enzyme genes. The genetic regulatory networks further modulate gene expression via transcription factors and epigenetic modifications, ensuring dynamic homeostasis of soluble sugar metabolism.

4.1. Key Enzyme Genes Involved in Soluble Sugar Metabolism in Fruits

The rapid advancement of molecular biology techniques has enabled the isolation of key enzyme genes involved in soluble sugar metabolism from diverse fruit species (Table 2). Nie et al. identified the PsSPS2 gene in the ‘Fengtang’ plum genome. Virus-induced gene silencing (VIGS) of PsSPS2 led to decreased sucrose content, indicating that this gene is crucial for sucrose accumulation and carbohydrate storage [48]. Bai et al. cloned the SPS-related gene MinSPS1 from ‘Guifei’ mango pulp, with its high expression during full ripening correlating with sucrose accumulation [49]. Studies on pineapple revealed differential expression of five SPS genes during fruit development. AcSPS5 was highly expressed in inflorescences, peel, and core, and is likely involved in sucrose accumulation and partitioning [50]. Wang et al. identified four lychee SPS genes; among them, LcSPS4 expression increases progressively with fruit growth and correlates positively with SPS activity and sucrose accumulation, establishing it as a key gene in sucrose biosynthesis [51]. Wei et al. demonstrated differential expression of four SPS genes in kumquat peel, with CsSPS4 expression increasing during fruit development, suggesting its role in sucrose accumulation and distribution during ripening [52]. In jackfruit, high expression levels of AhSPS1 and AhSPS2 suggest their critical regulation of sucrose content during fruit maturation [53]. Through whole-genome analysis, Zhang et al. identified seven SPS genes in apple; VIGS-mediated silencing of MdSPSA2.3 significantly reduced fruit sucrose content, confirming its role as a key carbohydrate accumulation gene [54].

Eleven SUS genes were discovered in the genome of apples. Among these, MdSUS2.1 and MdSUS1.4 increased during fruit development, which contrasted with the trends in enzyme activity. This observation suggests their involvement in sucrose metabolism and accumulation [55]. Abdullah et al. identified 30 SUS genes in pear, significantly exceeding the counts in citrus (6), kiwi fruit (9), grape (5), and peach (6). Among them, the PbSS5, PbSS3, and PbSS24 genes were highly expressed during fruit development, suggesting their potential key roles in sugar metabolism and development regulation [56,57,58,59,60]. Wang et al. identified five lychee SUS genes, including the known LeSUS1 and newly discovered LeSUS2-LeSUS5 [61]. In pitaya, the expression of SuSy5 and SuSy11 negatively correlated with sugar accumulation, indicating their regulatory function in soluble sugar synthesis [62]. Bao et al. identified five SUS genes in passion fruit, among which PeSUS3 displayed the highest expression in leaves and pericarp, suggesting its critical role in sucrose synthesis and transport [63]. Stroka et al. analyzed sugar metabolism genes during fruit ripening in ‘Gaucho’ (climacteric) and ‘Eldorado’ (non-climacteric). Their results revealed that CmSUS1 is associated with sucrose synthesis and accumulation in both varieties, while CmSUS2 showed high expression levels specific to ‘Gaucho’, potentially promoting its sucrose synthesis [64].

Six NINV genes were discovered in the genome of the pineapple, with AcNINV4 expression downregulated during fruit ripening, consistent with sucrose content changes [65]. They speculated that AcNINV4 might be a key enzyme in catalyzing sucrose degradation. Zhang et al. screened 17 sucrose metabolism-related genes in pitaya, among which HpVAI1 and HpNI4 showed positive correlations with VAI and NI activities, indicating their involvement in sugar metabolism regulation [66]. In red pitaya, HpVIN4 has the highest expression during ripening and a strong positive correlation with VIN activity, making it the main VIN gene [67]. Wang et al. identified 21 AIN genes from the highbush blueberry genome [68]. Nie et al. identified three INV genes in the genome of ‘Fengtang’ plum [48]. Jia et al. identified 31 INV genes in the kiwi fruit genome [58]. In pomegranate, PgINV3 and PgINV11 had significantly higher expression levels during fruit enlargement than during other periods, suggesting these genes may play a key role in fruit sucrose metabolism [69].

The complete SDH gene was cloned from the apple fruit [70], while Li et al. identified and characterized SDH and S6PDH genes across four rosaceae fruit trees (apple, pear, peach, and plum) [71]. SDH and S6PDH genes exhibited strong purifying selection, with a high frequency of optimal codons further underscoring this evolutionary influence. Du et al. identified a key gene, PsS6PDH4, in the genomes of ‘Fengtang’ plum and ‘April’ plum varieties. Following transient overexpression of PsS6PDH4 in strawberry, apple, and plum fruits, soluble solids and sorbitol accumulation were significantly enhanced, while its inhibition reduced these substances, highlighting the pivotal role of those genes in sugar metabolism in plum fruits [72].

The MdFRK2 gene was cloned from the apple genome, demonstrating its high substrate specificity for fructose, with a Km value of 0.1 mM, significantly exceeding MdFRK1’s affinity [73]. Chen et al. cloned the full-length cDNA of the FRK-related gene MrFRK2 from bayberry, noting its downregulation during late fruit ripening alongside rising fructose levels [74]. Lü et al. cloned FaFRK3 from the ‘Hongyan’ strawberry genome [75], which exhibited organ-specific expression patterns analogous to LbFRK7 in wolfberry and MrFRK2 in bayberry. Tao et al. cloned PpyFRK5 from pear [76], and Xie et al. cloned HpFRK1 from ‘Zihonglong’ pitaya. The latter specifically catalyzes cytoplasmic fructose phosphorylation but displays low affinity distinct from other plant FRKs, negatively regulating soluble sugar accumulation [77].

The MdHXK1 gene was cloned from the genome of ‘Gala’ apples, revealing its highest sequence homology with pear PbHXK1 and two conserved kinase domains (Hexokinase_1 and Hexokinase_2), which are critical for enzyme catalysis [78]. Zhao successfully cloned PbHXK1 from pear, observing its expression level peaking then declining during fruit development—a trend consistent with HXK activity dynamics [79]. In grape, Cakır identified six HXK genes, with VvHXK3 exhibiting high expression during fruit development and early maturation, suggesting its key role in glucose accumulation [80]. Shuai et al. successfully cloned the full-length cDNA sequence of DlHXK from longan, noting 82% similarity to ‘Wenzhou’ tangerine HXK. The gradual increase in DlHXK expression during fruit development implied its significance in sugar metabolism [81].

Table 2. Key enzyme genes related to soluble sugar metabolism in fruits.

Enzyme	Fruit	Gene Name	Reference
SPS	Plum	PsSPS2	[48]
	Mango	MinSPS1	[49]
	Pineapple	AcSPS1-5	[50]
	Litchi	LcSPS1-4	[51]
	Citrus	CsSPS1-4	[52]
	Jackfruit	AhSPS1-4	[53]
	Apple	MdSPSs	[54]
SUS	Apple	MdSUSs	[55]
	Pear	PbSSs	[56]
	Litchi	LeSUS1-5	[61]
	Yellow-skinned pitaya	SuSys	[62]
	Passion fruit	PeSUS1-5	[63]
	Muskmelon	CmSUS1, CmSUS2	[64]
INV	Pineapple	AcNINV1-6	[65]
	Red-fleshed pitaya	HpVIN1-4	[66]
	Blueberry	VcAINs	[68]
	Plum	PsNINV1, PsNINV3, PsNINV4	[48]
	Kiwi fruit	ArINVs	[58]
	Pomegranate	PgINV1-11	[69]
SDH	Peach	PpSDH1-3	[71]
	Apple	MdSDHs	[70]
S6PDH	Peach	PpS6PDH1, PpS6PDH2	[71]
	Plum	PsS6PDH4	[72]
	Apple	MdS6PDHs	[71]
FRK	Apple	MdFRK2	[73]
	Bayberry	MrFRK2	[74]
	Strawberry	FaFRK3	[75]
	Pear	PpyFRK5	[76]
	Pitaya	HpFRK1	[77]
HXK	Apple	MdHXK1	[78]
	Pear	PbHXK1	[79]
	Grape	VvHXK3	[80]
	Longan	DlHXK	[81]

Table 2. Key enzyme genes related to soluble sugar metabolism in fruits.

Enzyme	Fruit	Gene Name	Reference
SPS	Plum	PsSPS2	[48]
	Mango	MinSPS1	[49]
	Pineapple	AcSPS1-5	[50]
	Litchi	LcSPS1-4	[51]
	Citrus	CsSPS1-4	[52]
	Jackfruit	AhSPS1-4	[53]
	Apple	MdSPSs	[54]
SUS	Apple	MdSUSs	[55]
	Pear	PbSSs	[56]
	Litchi	LeSUS1-5	[61]
	Yellow-skinned pitaya	SuSys	[62]
	Passion fruit	PeSUS1-5	[63]
	Muskmelon	CmSUS1, CmSUS2	[64]
INV	Pineapple	AcNINV1-6	[65]
	Red-fleshed pitaya	HpVIN1-4	[66]
	Blueberry	VcAINs	[68]
	Plum	PsNINV1, PsNINV3, PsNINV4	[48]
	Kiwi fruit	ArINVs	[58]
	Pomegranate	PgINV1-11	[69]
SDH	Peach	PpSDH1-3	[71]
	Apple	MdSDHs	[70]
S6PDH	Peach	PpS6PDH1, PpS6PDH2	[71]
	Plum	PsS6PDH4	[72]
	Apple	MdS6PDHs	[71]
FRK	Apple	MdFRK2	[73]
	Bayberry	MrFRK2	[74]
	Strawberry	FaFRK3	[75]
	Pear	PpyFRK5	[76]
	Pitaya	HpFRK1	[77]
HXK	Apple	MdHXK1	[78]
	Pear	PbHXK1	[79]
	Grape	VvHXK3	[80]
	Longan	DlHXK	[81]

4.2. The Signal Response Mechanism of Key Enzyme Genes

Soluble sugars in fruits constitute core components determining flavor and nutritional value. Their accumulation is precisely regulated by complex signal response mechanisms, with research focus evolving from single-enzyme gene functions to integrated analysis of multi-dimensional signal networks. Molecular mechanisms governing key sugar-metabolizing enzymes span multiple levels, including hormone signaling and environmental interactions, with significant variation in complexity across species.

Plant hormones, as key bioactive compounds in plants, regulate fruit growth and development by modulating sugar metabolism. Specifically, abscisic acid (ABA), gibberellin (GA), auxin (IAA), ethylene (ETH), etc., are greatly involved. Studies have found that ABA and GA3 coordinately regulate the expression of key sugar metabolism genes (e.g., VvCWINV and VvGIN) in grape berries, upregulating their activity during the leaf and berry coloration period to enhance sugar transport from leaves to fruits [82]. Additionally, exogenous GA3 elevates total sugar content by strengthening carbon sink capacity and balancing hormone levels—increasing GA, IAA, and CTK while reducing ABA [83]. Hong et al. found that ABA, as a maturity hormone, participates in regulating fruit coloring and sugar accumulation. In grapes, exogenous ABA upregulates VvSS3 expression but inhibits VvSnRK1β at high concentrations, revealing a dynamic balance in ABA signaling. At the same time, VvSS3 overexpression enhances ABA synthesis genes (VvNCED1, VvZEP) and ABA pathway-related genes [84]. Under source limitation, ABA further increases fruit sugar accumulation by regulating HT1 expression [85]. In apples, ETH promotes starch degradation by activating enzymes (SPS, AINV, CWINV) and by inducing the expression levels of MdSPS, MdSUSYS, MdAINV, MdNINV, and MdCWIN [86]. In plums, ETH reduces sucrose catabolism while stimulating sorbitol breakdown [87]. Wang et al. found that exogenous ETH downregulates sucrose synthesis genes (VcSPS1, VcNIN2) but upregulates decomposition genes (VcSS1, VcCWINV1), reducing sucrose while accumulating glucose and fructose [88]. Melatonin (MT) was found to enhance key genes involved in sugar metabolism enzymes, while partially inhibiting the SDH gene. This delays sucrose and sorbitol degradation in peaches, leading to increased sugar content [89].

Sugar is vital for fruit tree development, serving not only as an energy source but also as a signaling molecule that regulates gene expression in response to environmental stimuli, thereby controlling flower and fruit ripening [90]. Soluble sugars enhance plant cold resistance by acting as osmolytes to protect cells during chilling stress. Wang et al. transiently overexpressed the invertase inhibitor (INH) gene PpINH1 in peach fruits and found that it significantly reduced vacuolar invertase (VIN) activity by directly binding to PpVIN2, while concurrently increasing sucrose content and cold tolerance [91].

Temperature and drought jointly affect sugar accumulation in jujube fruits: elevated temperatures increase sugar content, whereas drought reduces it, clarifying jujube quality responses under current climate warming [92]. Additionally, drought also promotes soluble sugar accumulation. These sugars help maintain membrane–protein hydrophilic interactions by substituting for water molecules, prevent protein denaturation, and protect cell structures by forming an amorphous glass matrix. As signaling molecules, sugars participate in stress perception and signal transduction, modulating carbohydrate metabolism genes [93]. Citrus fruits accumulate more soluble sugars under drought stress. Drought treatment upregulates the expression of key genes but downregulates SUS2, SUS5, SUS6, SPS3, and NIV4, simultaneously boosting sugar accumulation and drought resistance [94].

Moderate shading improves leaf photosynthetic capacity, mitigates photoinhibition, and thereby improves fruit quality [95]. For example, intercropping mango with pineapple under shading treatment increased the total soluble sugar content [96]. The latest research has found that short-day shading further upregulates soluble sugar metabolism genes (e.g., CwINV6, CwINV7, and CsSUS6), facilitating photosynthate transport from leaves to fruits, while inducing starch degradation-related genes to convert starch into cytoplasmic soluble sugars. This dual mechanism promotes both sugar accumulation and cold resistance [97].

Plant nutrients, primarily absorbed by roots from soil, play a key role in growth and development, with nitrogen (N) being an essential element influencing fruit quality. Moderate salt stress enhances sugar metabolism-related genes in figs, promoting the synthesis of sucrose and sorbitol [98]. Nitrogen application during fruit ripening upregulates MdSPS1, MdSPS6, MdFRK2, and MdHXK1 genes in ‘Fushi’ apple fruits, promoting the conversion of fructose and glucose, and results in an increase in sucrose. This alters soluble sugar composition by reducing hexose content and increasing sucrose accumulation. Consequently, such shifts diminish fruit sweetness and overall quality, indicating that nitrogen should not be applied before fruit harvest [99].

4.3. Key Enzyme Gene Genetic Regulatory Network

The metabolic pathway of soluble sugars in fruits involves a complex network requiring coordinated expression of multiple sugar metabolism genes, mediated by transcription factors and epigenetic modifications. This study collectively describes the genetic regulatory network governing key enzymatic genes by analyzing transcription factors and epigenetic mechanisms, thereby advancing understanding of the molecular regulation of sugar accumulation. These insights will highlight potential regulatory mechanisms and potential strategies for manipulating key enzymatic genes to enhance fruit sugar content.

The regulation of sugar metabolism in fruits involves a complex gene regulatory network, namely various transcription factor (TF) families. Key TF families—NAC, MYB, WRKY, bHLH, and bZIP—critically influence fruit sugar accumulation by interacting with sugar metabolism-related genes. The latest research has found that in strawberries, the NAC transcription factor FvNAC073 is upregulated during ripening and can directly activate the sucrose-6-phosphate synthase gene (FvSPS1) to promote sucrose synthesis [100]. In apples, MdNAC5 binds the promoters of MdTST2 and MdNINV6, enhancing vacuolar fructose accumulation and sucrose-to-fructose conversion [101]. Wei et al. found that in bananas, MaNAC19 directly binds to the MaSPS1 promoter, activating its expression to promote sucrose synthesis. Conversely, MaXB3 inhibits this process via ubiquitin-mediated degradation of MaNAC19 [102]. In citrus, CsWRKY2 and CsWRKY20 activate CsSPS2 to promote sugar accumulation, while CsWRKY28 inhibits accumulation through ubiquitination, which promotes the degradation of MaNAC19 and reduces sucrose synthesis [103]. Zhang et al. found that in apple, the overexpression of MdWRKY126 upregulated sucrose-synthesis genes while downregulating degradation genes, leading to increased sucrose but reduced glucose and fructose contents [104]. MdbHLH3 increases photosynthetic capacity and carbohydrate levels in leaves and enhances carbohydrate accumulation in fruits by regulating the distribution of carbohydrates from source to sink [105]. In pear, PbrbZIP15 activates PbrXylA1 to boost soluble sugar accumulation [106]. In apple and other rosaceae fruit trees, SnRK1 integrates sucrose signaling and sorbitol response by phosphorylating bZIP39. This process orchestrates the expression of sorbitol metabolism genes (MdSDH1, MdA6PR) according to energy status [107]. Moreover, in apple, MdSDH2 has a SNP variation in the promoter region that affects the binding ability of transcription factor MdABI3, where the adenine nucleotide promoter exhibits stronger binding to MdABI3 [108]. Transcription factor CitZAT5 in citrus synergistically interacts with CitNAC47 to enhance CitSUS5 promoter activity, accelerating sucrose-to-hexose conversion. CitZAT5 expression levels are positively correlated with hexose content, underscoring its crucial role in regulating sucrose accumulation and the hexose ratios. This mechanism offers potential genetic targets for improving citrus sweetness and quality [109].

Epigenetic regulation plays a crucial role in silencing transposable elements and maintaining appropriate gene expression to regulate various biological processes. In this context, epigenetic modifications, including DNA methylation, histone modifications, and non-coding RNAs, significantly influence sugar metabolism in fruits. Ma et al. found that increased DNA methylation levels profoundly reduced soluble sugar accumulation in apple fruits [110]. Yang et al. identified DNA methylation-regulated expression of sugar metabolism genes (e.g., CINV1 and SPP2) during melon fruit development [111]. Additionally, DNA demethylation reduces sugar content during the development process of grapes [112]. These epigenetic alterations impact histone–DNA/protein interactions, either promoting or repressing gene activity. Studies have found that transcription factor PuWRKY31 positively regulates sucrose transporter PuSWEET15 by binding to its promoter, thereby affecting sucrose accumulation in pears. Concurrently, the histone acetylation level of the PuWRKY31 promoter affects its expression, thereby influencing sucrose accumulation [113]. Moreover, we also explored the role of histone deacetylation in regulating fruit sugar metabolism. The latest research found that transcription factors PuPRE6, PuMYB12, and histone deacetylase PuHDAC9-like regulate soluble sugar accumulation. PuMYB12 and PuPRE6 act as antagonistic complexes to regulate the transcription of sucrose transporter PuSUT4-like, while histone acetylation levels of PuMYB12 and PuSUT4-like affect their expression, thereby influencing sucrose accumulation in pear fruits [114]. Vall-llaura et al. found that the histone deacetylation gene SRT is critical for pear sugar metabolism, with PbSRT2 positively correlating with sugar accumulation, indicating epigenetic targeting during fruit ripening [115]. Non-coding RNAs also participate in fruit sugar metabolism. For example, differentially expressed long non-coding RNAs (lncRNAs) contribute to fruit development and carbohydrate accumulation [116], with similar function as implicated in apple quality formation [117]. In wolfberry, miR156 regulates sucrose metabolism-related genes FRK, thereby affecting soluble sugar accumulation [118].

5. Conclusions and Outlook

Soluble sugars critically influence fruit flavors and quality formation through complex metabolic networks. We systematically reviewed the accumulation patterns of soluble sugars in fruits, the spatiotemporal distribution of key enzyme activities during fruit development, the functional identification of key enzyme genes, and the signal response mechanisms and genetic regulatory networks. Comparative analysis across species reveals conserved and divergent sugar metabolism traits, advancing our understanding of flavor formation mechanisms. While current studies have revealed the functions of some fruit sugar metabolism-related genes, their expression regulation in response to varying environmental conditions and developmental stages requires deeper exploration. Based on previous research results, several ideas are proposed for future research:

(1)

Further investigation is required into the specific signaling pathways regulating key enzymes involved in sugar metabolism, particularly the interactions among environmental factors, endogenous hormones, transcription factors, and epigenetic modifications. Experimental designs could incorporate environmental and hormonal interactions to monitor phenotypic responses, combined with multi-omics approaches such as methylomics, transcriptomics, and metabolomics to dynamically capture changes in relevant regulatory factors. Integrative multi-omics analysis can identify key regulatory nodes, thereby elucidating interaction networks that may serve as a foundation for improving fruit quality.

(2)

A comprehensive understanding of the molecular network of sugar metabolism requires integrating multi-omics technologies, genetic engineering, and computational modeling. For the same fruit material, transcriptomic, proteomic, and metabolomic data should be collected simultaneously across different developmental stages or in mutant lines. Using Weighted Gene Co-expression Network Analysis (WGCNA), we can identify gene modules and protein–metabolite interaction pairs significantly correlated with sugar content. Functional validation of core genes can then be achieved through gene knockout or overexpression experiments. Based on multi-omics datasets, systems biology tools can be applied to construct dynamic models incorporating key enzymes, transporters, and regulatory factors. These models simulate shifts in sugar metabolic flux under varying conditions and are then validated through in vitro metabolic assays.

(3)

Given the close relationship between sugar metabolism and other plant metabolic pathways, targeted analysis should focus on identifying key intersection points between sugar metabolism and secondary or energy metabolism. Isotope labeling techniques can trace carbon flux, which, combined with metabolite correlation analysis, helps pinpoint critical cross-regulatory nodes. This approach facilitates the identification of co-regulatory factors influencing both sugar metabolism and other pathways. Subsequently, yeast two-hybrid screening can detect interacting proteins. Chromatin immunoprecipitation sequencing (ChIP-seq) can determine the binding sites of these regulators on genes within different metabolic pathways, thereby clarifying the molecular mechanisms by which a single regulatory factor coordinates multiple pathways. This will deepen our understanding of the interplay between sugar metabolism and other metabolic processes.

(4)

The distinct patterns of sugar metabolism observed across fruit species reflect their evolutionary strategies for environmental adaptation. Future studies should explore the role of sugar metabolism in ecological and evolutionary adaptation in plants. Comparative analyses of sugar metabolism phenotypes between cultivated varieties and their wild relatives can reveal evolutionarily conserved, quality-associated genes. These genes can serve as molecular markers in hybrid breeding programs. Consequently, marker-assisted selection can be applied to precisely improve fruit sugar content and environmental resilience, thus offering novel insights for fruit tree breeding and cultivation practices.