Incomplete functional divergence drives genetic synergy during floral development in tomato

Abstract

Genetic synergy arises from interactions between functionally related genes that control complex traits in plants and animals. Synergy occurs when the combined effect of multiple genes exceeds the additive contribution from each individual gene. However, genetic mechanisms that drive and maintain synergy remain largely elusive. Here, we investigated synergistic interactions among SEPALLATA MADS-box genes during floral development in tomato. We discovered that synergy emerges from duplicated genes that partitioned functions to regulate inflorescence architecture and floral organ identity. Moreover, synergistic interactions are reflected in non-additive expression changes that coordinate successive developmental stages. Finally, we demonstrate that synergy occurs due to residual redundancy on a dose-sensitive module guiding floral identity. These results indicate that synergy emerges as a relic of redundancy when functional divergence remains incomplete due to gene dosage constraints. Our work provides insights into mechanisms through which gene families diverge to produce the substrate for biological innovations during evolution.