Solanaceae pan-genomes reveal extensive fractionation and functional innovation of duplicated genes.

Abstract

The Solanaceae family contains many agriculturally important crops, including tomato, potato, pepper, and tobacco, as well as other species with potential for agricultural development, such as the orphan crops groundcherry, wolfberry, and pepino. Research progress varies greatly among these species, with model crops like tomato being far ahead. This disparity limits the broader agricultural application of other Solanaceae species. In this study, we constructed an interspecies pan-genome for the Solanaceae family and identified various gene retention patterns. Our findings reveal that the activity of specific transposable elements is closely associated with gene fractionation and transposition. The pan-genome was further resolved at the level of T subgenomes, which were generated by Solanaceae-specific paleo-hexaploidization (T event). We demonstrate substantial gene fractionation (loss) and divergence events following ancient duplications. For example, all class A and E flower model genes in Solanaceae originated from two tandemly duplicated genes, which expanded through the γ and T events before fractionating into 10 genes in tomato, each acquiring distinct functions critical for fruit development. Based on these results, we developed the Solanaceae Pan-Genome Database (SolPGD, http://www.bioinformaticslab.cn/SolPGD), which integrates datasets from both inter- and intra-species pan-genomes of Solanaceae. These findings and resources will facilitate future studies of solanaceous species, including orphan crops.