Spatial control of anthocyanin and proanthocyanidin production in tomato fruits by competitive MBW complexes to promote seed dispersal

Anthocyanins and proanthocyanidins (PAs) are flavonoid compounds with important roles in plant physiology and ecology, as well as beneficial effects on human health. Although they share a common biosynthetic pathway, these two types of flavonoids exhibit different tissue-specific accumulation patterns in many fruits and plant organs. In tomato, anthocyanins accumulate primarily in the fruit peel of some wild relatives, whereas PAs accumulate mainly in seeds. However, the molecular mechanisms that underlie these patterns remain to be characterized. Here, we demonstrate that the tissue-specific accumulation of anthocyanins and PAs in tomato fruits is governed by different MYB-basic helix-loop-helix (bHLH)-WD40 (MBW) transcriptional modules. The bHLH transcription factor SlAN1 and the WD40 regulator SlAN11, critical components of the MBW complex, are required for both anthocyanin and PA biosynthesis. By contrast, two MYB components of the MBW complex, SlAN2-like and SlMYB54, specifically regulate anthocyanin biosynthesis in the peel and PA biosynthesis in seeds, respectively. The two MYB components interact with SlAN1 to form two competitive MBW transcriptional modules that control the tissue-specific accumulation of anthocyanins and PAs in tomato fruits. Finally, we provide evidence that these tissue-specific accumulation patterns are likely orchestrated by a dual-layered protective mechanism to ensure successful seed dispersal. Our findings reveal that efficient biosynthesis of anthocyanins and PAs arises from strict tissue-specific expression of both regulatory and functional genes, suggesting strategies for the enhancement of anthocyanin and PA levels in tomato fruits.