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

Anthocyanins and proanthocyanidins (PAs) are important flavonoids that have beneficial effects on plants and human health. Despite partially sharing a common biosynthetic pathway, these two flavonoids have a preference for tissue-specific accumulation in many fruits and plant organs. In tomato, anthocyanins are primarily accumulated in fruit peel of some wild relatives, while PAs are mainly accumulated in seeds. However, the underlying molecular mechanisms remain elusive. Here, we demonstrated that the tissue-specific accumulation of these two flavonoids in tomato fruits was achieved by different MYB-bHLH-WD40 (MBW) transcriptional modules. The bHLH transcription factor SlAN1 and the WD40 regulator SlAN11, critical components in the MBW complex, were required for both anthocyanin and PAs biosynthesis. By contrast, two MYB components of the MBW complex, SlAN2-like and SlMYB54, specifically regulated anthocyanins biosynthesis in peel and PAs biosynthesis in seeds, respectively. We further found that the two MYB components interacted with SlAN1 to form two competitive MBW transcriptional modules for tissue-specific accumulation of anthocyanins and PAs in tomato fruits. We also provided evidence supporting that the tissue-restricted accumulation pattern of anthocyanins and PAs in tomato fruit likely orchestrated a dual-layered protective mechanisms for successful seed dispersal. Our findings exemplified that the efficient biosynthesis of anthocyanins and PAs was attributed to the strict tissue-specific expression of both regulatory and functional genes, which provided a strategy to enhance anthocyanins and PAs levels in tomato fruits.