An InDel in the Promoter of Selected during Tomato Domestication Determines Fruit Malate Contents and Aluminum Tolerance.

Deciphering the mechanism of malate accumulation in plants would contribute to a greater understanding of plant chemistry, which has implications for improving flavor quality in crop species and enhancing human health benefits. However, the regulation of malate metabolism is poorly understood in crops such as tomato (). Here, we integrated a metabolite-based genome-wide association study with linkage mapping and gene functional studies to characterize the genetics of malate accumulation in a global collection of tomato accessions with broad genetic diversity. We report that (tomato fruit malate 6), which corresponds to (Sl in tomato), is the major quantitative trait locus responsible for variation in fruit malate accumulation among tomato genotypes. A 3-bp indel in the promoter region of Sl was linked to high fruit malate content. Further analysis indicated that this indel disrupts a W-box binding site in the Sl promoter, which prevents binding of the WRKY transcription repressor Sl-WRKY42, thereby alleviating the repression of Sl expression and promoting high fruit malate accumulation. Evolutionary analysis revealed that this highly expressed Sl allele was selected for during tomato domestication. Furthermore, vacuole membrane-localized Sl-ALMT9 increases in abundance following Al treatment, thereby elevating malate transport and enhancing Al resistance.