Advance in research on the regulation of fruit sugar accumulation and quality formation in horticultural crops by sugar transporters

Fruit quality is a core determinant of the economic value of horticultural crops and consumer acceptance, with sugar content and composition being key indicators for evaluating flavor quality. During fruit development, photosynthetic products are primarily transported as sucrose to the fruit via the phloem. Unloading occurs through the apoplastic or symplastic pathway, and sugars are ultimately stored in the vacuoles of flesh cells. This complex process relies on the precise and coordinated regulation of various sugar transporters. In recent years, with the rapid development of molecular biology techniques, researchers have identified three major classes of key sugar transporter families in horticultural crops such as apple, grape, citrus, strawberry, pitaya, and tomato: SWEET proteins, as novel unidirectional transporters, mediate sugar efflux through their unique 7-transmembrane domain structure forming dimers, playing a crucial role in apoplastic unloading, for example, watermelon ClSWEET3 is responsible for unloading sucrose from the phloem companion cells into the apoplastic space; Sucrose Transporters (SUTs) act as H+ /sucrose cotransporters, utilizing a proton gradient to drive active sucrose transport, and can be classified into types Ⅰ-Ⅲ based on affinity differences, serving important func-tions in phloem loading and unloading, for instance, the expression of tomato LeSUT2 is closely related to the sucrose unloading efficiency; vacuolar sugar transporters (TSTs) are localized in the tonoplast and act as the“final checkpoint”for sugar storage, whose activity is positively correlated with sugar content in storage organs, for example, the natural variation in the promoter of watermelon ClTST2 during domestication significantly could enhance fruit sweetness. These transporters, through functional differentiation and synergistic interaction, collectively form the molecular basis for sugar accumulation in the fruits. Among them, the SWEET and SUT families are primarily involved in transmembrane transport and allocation of sugars, while the TST family dominates vacuolar storage, together forming a complete“unloading- absorption- storage”cascade pathway. Regarding molecular regulatory mechanisms, the expression and activity of sugar transporters are intricately controlled by a multi-layered network. At the transcriptional level, various transcription factors achieve spatiotemporal expression regulation through specific binding to cis-elements, for example, in citrus, CsMYB36 regulates the expression of the CsSWEET17 via the calcium signaling pathway, and in grape, VvNAC72 activates the VvSWEET15 expression at the veraison stage; at the post-transcriptional and post-translational levels, modifications such as phosphorylation and ubiquitination dynamically regulate protein activity and stability, for instance, the phosphorylation status of the Arabidopsis AtSWEET11/12 is regulated by drought stress, and the potato E3 ubiquitin ligase StRFP1 regulates sugar partitioning by degrading the StSWEET10c/11; the epigenetic regulation influences gene expression through DNA methylation and histone modifications, such as the expression of melon CmTST2 being dynamically regulated by the methylation level of its promoter region; plant hormones like ABA and ethylene precisely regulate sugar transporter function through complex signaling networks that integrate internal and external signals, for example, ABA promotes soluble sugar accumulation in tomato by activating AREB2; environmental factors such as drought, salinity, and low temperature stress reprogram sugar transporter function through specific signaling pathways, for instance, in apple, ABA activates MdCIPK22 leading to phosphorylation of the MdSUT2.2, enhancing its transport activity. Notably, sugar transporters not only directly regulate sugar accumulation but also influence fruit quality through synergistic interactions with sugar-metabolizing enzymes. For example, increased activity of tomato SlCWIN upregulates the expression of the SlHT2 and SlSWEET12c, and grape VvNAC72 simultaneously activates the expression of the VvSWEET15 and sucrose phosphate synthase (VvSPS), forming a“metabolism-transport”coupling mechanism. Furthermore, sugar transporters indirectly affect multiple fruit quality traits such as size, color, and aroma through sugar signaling pathways. For instance, the overexpression of the tomato SlSWEET12c simultaneously increases sugar content and promotes fruit coloration, demonstrating its pleiotropic regulatory characteristics. Based on current research progress, future fruit quality improvement should focus on the following directions: In-depth mining of allelic variation in germplasm resources, screening for natural variants regulating the key sugar transporters using population genetics methods, and developing efficient molecular markers; Deciphering the coordinated regulatory network of quality traits, revealing the interaction mechanisms between sugar transporters and pathways involved in organic acid metabolism, color formation, etc.; Innovating genetic improvement strategies, utilizing precise promoter editing technologies to achieve accurate spatiotemporal dynamic regulation of sugar transporter expression, avoiding source-sink relationship imbalance; Exploring modular breeding, using synergistic“metabolism- transport”functional modules as breeding units for multi- gene co- transformation; Strengthening the discovery and functional exploration of novel sugar transporters (e.g., H+ -coupled glucose transporters, HGT; sucrose transport- related proteins, SRT) in fruit quality regulatory networks,which are garnering increasing attention. For instance, although HGTs have been studied earlier in model plants, their functional research in horticultural crop fruits is still at the forefront. Their mechanism of utilizing proton gradients to drive monosaccharide transport might provide an important“backup pathway”for active sugar uptake during early fruit development or under stress conditions. The genetic evidence for another class, Sucrose Transport-Related Proteins (SRTs), also hints at their non- redundant role in sucrose transport and partitioning. However, current understanding of the expression patterns, substrate specificity, and physiological functions of these novel transporters in fruits remains very limited. Future research urgently needs to combine genomics, structural biology, and gene editing technologies to systematically identify their family members and decipher their precise biochemical functions and regulatory mechanisms, thereby revealing their unique contributions to the fruit sugar accumulation network and opening new theoretical foundations and genetic targets for quality improvement. Translating these basic research findings into cultivation practices will involve regulating sugar transporter expression through optimized management of light, temperature, water, and fertilizer, while simultaneously breeding climate- resilient cultivars capable of maintaining normal sugar transport under climate change backgrounds. Systematically analyzing the regulatory network of sugar transporters not only deepens the understanding of the mechanisms underlying fruit quality formation but also provides new targets and technical pathways for molecular breeding of fruit trees, holding significant importance for achieving precise improvement of fruit quality.