All-flesh fruit in tomato is controlled by reduced expression dosage of AFF through a structural variant mutation in the promoter.

ABSTRACT

The formation of locule gel is an important process in tomato and is a typical characteristic of berry fruit. In this study, we examined a natural tomato mutant that produces all-flesh fruit (AFF) in which the locule tissue remains in a solid state during fruit development. We constructed different genetic populations to fine-map the causal gene for this trait and identified SlMBP3 as the locus conferring the locule gel formation, which we rename as AFF. We determined the causal mutation as a 416-bp deletion in the promoter region of AFF, which reduces its expression dosage. Generally, this sequence is highly conserved among Solanaceae, as well as within the tomato germplasm. Using BC6 near-isogenic lines, we determined that the reduced expression dosage of AFF did not affect the normal development of seeds, whilst producing unique, non-liquefied locule tissue that was distinct from that of normal tomatoes in terms of metabolic components. Combined analysis using mRNA-seq and metabolomics indicated the importance of AFF in locule tissue liquefaction. Our findings provide insights into fruit-type differentiation in Solanaceae crops and also present the basis for future applications of AFF in tomato breeding programs.