Integrated transcriptome and metabolome analysis reveal SeAPRR2 as the key regulator controlling fruit quality in green and white chayote

Fruit color polymorphism in chayote, ranging from dark green to white, is closely associated with nutritional quality. However, the underlying molecular mechanisms remain poorly understood, particularly in white-fruited accessions. This study integrated phenotypic, transcriptomic, metabolomic, and functional analyses using four fruit color morphotypes: dark green (DGF), green (GF), light green (LGF), and white (WF). Physiological traits, including chlorophyll and nutrient contents, were quantitatively assessed. Transcriptomic and metabolomic profiles were generated using Illumina sequencing and LC-MS/MS, respectively. Functional validation was performed by overexpressing SeAPRR2 in tomato. The results showed that WF exhibited significantly reduced chlorophyll content, lower soluble sugar and soluble protein levels, but the highest soluble solids content. Transcriptomic analysis identified 1255 common differentially expressed genes (DEGs) between pigmented and white fruits, which were primarily enriched in photosynthesis-related pathways (e.g., light-harvesting complex (LHC) and photosystem I/II (PSI/PSII) genes) and carbohydrate metabolism pathways (e.g., sucrose synthase (SUS) and invertase (INV)). Metabolomic profiling detected 1250 metabolites, with photosynthetic intermediates such as sucrose and trehalose-6-phosphate significantly reduced in WF. Notably, the transcription factor SeAPRR2 was silenced in WF, while its overexpression in tomato significantly enhanced chlorophyll, sugar, and starch content. This study demonstrates that white fruits lose photosynthetic capacity due to impairments in the light-harvesting complex and sucrose metabolism, thus relying on photoassimilates imported from leaves. SeAPRR2 acts as a core regulator that enhances fruit quality by promoting chloroplast development. These findings elucidate the molecular link between fruit color and quality in chayote and provide a theoretical basis for marker-assisted breeding. • Multi-omics reveals metabolic reprogramming to starch storage in white chayote fruits, driven by suppressed sucrose synthesis. • White chayote fruits exhibit a complete loss of photosynthesis, becoming dependent on leaf-derived photoassimilates. • SeAPRR2 is a master regulator of fruit quality, enhancing nutritional traits in transgenic tomato.