Background This study assessed the effects of auxin analog, para-chlorophenoxyacetic acid (pCPA), on fruit set and development in Micro-Tom tomato (TOMJPF00001) via phenotypic, biochemical, metabolomic, and transcriptomic analyses. Results pCPA treatment significantly (p < 0.05) reduced floral abscission, increased fruit set and yield, while impacting fruit morphology, ripening, sugar content, organoleptic properties, and phytohormone profiles. Metabolomic profiling revealed 836 differentially accumulated metabolites (DAMs). Among these, several phenylpropanoid-related DAMs (isoferulic acid, 6-methylcoumarin, naringenin, hesperetin 5-O-glucoside, quercetin, and dihydrokawain) were upregulated in immature green, mature green, and breaker fruits, but downregulated in red ripe fruits following pCPA application. Transcriptome analysis yielded 35,501 differentially expressed genes (DEGs), including 740 novel genes, with growth stage-specific expression patterns observed in phenylpropanoid, carotenoid, and flavonoid biosynthetic pathways. Particularly, pCPA treatment downregulated chitinase (Soly04g072000.3) and acidic endochitinase (Soly05g050130.3), potentially enhancing fruit firmness through cell wall stabilization. Reduced accumulation of alpha-L-arabinofuranosidase (Soly10g077080.2) and a UDP-glucose 6-dehydrogenase family protein (Soly06g069550.1) further supported this observation. In red ripe fruits, pCPA decreased organic acids (malic and citric acids), sugars (fructose, glucose and sucrose), soluble solids (TSS/brix), amino acids (aspartic acid, phenylalanine, valine) and nucleotide (uracil, cytosine) levels, correlating with altered sensory attributes. pCPA also influenced lipid biosynthesis in mature green fruits and consistently downregulated sucrose across all developmental stages, suggesting impacts on carbohydrate metabolism. Furthermore, pCPA treatment altered the expression of genes related to carbohydrate metabolism, including beta-amylase (Soly08g007130.3), ADP-glucose pyrophosphorylase (Soly07g056140.3), and beta-glucosidase (Soly11g071640.2). pCPA-induced alterations in fruit development were correspondingly susceptible to alternative splicing patterns. Conclusions These findings provide insights into the molecular mechanisms underlying pCPA-induced changes in tomato fruit set and development, offering valuable information for optimizing horticultural breeding practices and strategies.

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