All-Flesh Tomato Regulated by Reduced Expression Dosage of AFF Through a Promoter SV Mutation.

The formation of locule gel is an important process in tomato and a typical characteristic of berry fruit. In this study, we collected a tomato natural mutant that produces all-flesh fruits (AFF) in which the locule tissue remains in a solid state during fruit development. We built genetic populations to fine-map the causal gene of the AFF trait and identified the gene AFF (SlMBP3) as the locus conferring the locule gel formation. We determined the causal mutation as a 416-bp deletion that occurred in the promoter region of AFF and reduced its expression dosage. The 416-bp sequence is highly conserved among Solanaceae species, as well as within the tomato germplasm. Furthermore, with the BC6 NIL materials, we revealed that the reduced expression dosage of AFF did not impact the normal development of seeds but produced unique non-liquefied locule tissue, which was distinct from that of normal tomatoes in terms of metabolic components. We further revealed the importance of AFF gene in locule tissue liquefaction through combined analysis using mRNA-seq and metabolomics. Our findings provide clues to investigate fruit type differentiation in Solanaceae crops and also contribute to the application of the AFF gene in tomato breeding programs.