Pepper variome reveals the history and key loci associated with fruit domestication and diversification

Pepper (Capsicum spp.) is one of the earliest domesticated crops, providing a unique pungent sensation when eaten. Through the construction of the first pepper variome, we describe the main groups that emerged during domestication and breeding of C. annuum, their relations and temporal succession, and the molecular events underlying the main transitions. The initial differentiation in fruit shape and pungency, increase in fruit weight, and transition from erect to pendent fruits, and the recent appearance of blocky, large, sweet fruits (bell peppers), were accompanied by strong selection/fixation of key alleles and introgressions in two large genomic regions. Furthermore, we describe the identification of Up, a key domestication gene controlling erect vs pendent fruit orientation, encoding a BIG GRAIN protein involved in auxin transport, and Flip1 associated with capsaicinoid content, encoding a protein involved in phospholipid flipping. The function of Up was confirmed by virus-induced gene silencing. These findings constitute a cornerstone for understanding the domestication and differentiation of a key horticultural crop.