Male sterility-induced parthenocarpy arose during tomato domestication

The huge diversity of cultivated tomatoes is the result of a long process of domestication followed by intensive breeding. Breeding efforts have been focused on increasing fruit size and on the diversification of fruit phenotypes. The formation of seedless (parthenocarpic) fruits in tomato plants is an interesting trait for growers, providing a mechanism to overcome fertilization failure under unfavourable environmental conditions. Early anther or pollen ablation is an effective strategy to promote parthenocarpy in tomato plants and was proven to be effective in several tomato cultivars. Whether this is an ancestral trait or was acquired during domestication and breeding is unknown. In this study, we evaluated the formation of parthenocarpic fruits in the cultivated tomato and the wild relative Solanum pimpinellifolium through the generation of male-sterile mutants. Only cultivated tomatoes, but not Solanum pimpinellifolium plants, produced seedless fruits. Expression analyses showed that parthenocarpy correlates with the activation of fertilization-independent gibberellin biosynthesis in the ovaries. When compared with wild relatives, modern tomato cultivars present small deletions in the promoter of these genes that could account for the differences in gene expression that ultimately trigger parthenocarpy. Our results suggest that seedless fruit production was actively repressed in the absence of pollination in the ancestral tomato lineages.