The TANG cluster comprising 10 nitrate transporter genes controls fruit sweetness and size in tomato

Sucrose is a major transport form of photoassimilated carbon in tomato, Arabidopsis, and many other plant species and plays a critical regulatory role in plant growth, development, and fruit quality. Plant vacuoles function as storage organelles, accumulating substantial quantities of metabolically inactive nitrates as a nitrogen reserve and soluble sugars as a carbon reserve. Consequently, the balance between nitrate and sucrose accumulation determines plant growth dynamics and fruit taste. In this study, we identified a gene cluster designated TANG (Total soluble solids accumulation via nitrate transporter gene cluster), comprising 10 nitrate transporter genes that are significantly associated with sucrose accumulation in tomato. This gene cluster mediates nitrate transport between the cytoplasm and vacuole, thereby influencing its storage. Functional disruption of TANG8, a member of this gene cluster, results in either enhanced sugar accumulation or increased fruit size. Selective disruption of multiple TANG cluster members yields fruits with elevated sweetness and increased fruit size in Solanum pimpinellifolium. The interaction between TANG members and tonoplast-localized sucrose transporter 4 implies a possible mechanism underlying competitive accumulation of nitrate and sugar in tomato. Collectively, our work not only identifies a gene cluster controlling tomato fruit sweetness and size but also provides a strategy of engineering crops for high quality and yield through multiplex editing of the gene cluster.