Remodeling of the tuberization-controlling FLOWERING LOCUS T genes from non-tuberizing ancestor to potato

Potato (Solanum section Petota) originated from a natural hybridization between tomato and Etuberosum ancestors, through which the trait of tuber formation evolved. Genetically, tuberization in potato is controlled by FLOWERING LOCUS T (FT) homologs. However, from non-tuberous ancestors to potato, what remodeling of these tuber formation determinants emerged remains unclear. Using homology-based discovery, expression profiling, CRISPR knockouts, and genetic complementation, we here show that tuberization-controlling FT-like genes underwent Petota-specific expansion, restructuring, and divergence at key functional residues. We found that short day-induced SeSP5G expression inhibited flowering of Etuberosum, a non-tuberous ancestor. This thereby defines it as a long-day plant (LDP) and suggests that the short day-dependent tuberization of potatoes was likely an inheritance from Tomato. Importantly, by expressing the potato tuber-forming gene StSP6A in Solanum etuberosum, which forms underground stems but is hypothesized to lack tubers from pseudogenization of the SeSP6A gene, we show that the complementation of StSP6A promotes floral transition in Etuberosum yet fails to induce tuber development. Thus, it is indicated that the key genetic determinants enabling tuberization downstream of SP6A diverge between Petota and Etuberosum. These studies identify key renovations in FT-like genes that facilitate the recruitment of the florigenic signaling for tuberization, exemplifying speciation-driven functional innovation in a widely conserved gene.