Dynamic evolution of small signaling peptide compensation in plant stem cell control

Abstract: Gene duplications are a hallmark of plant genome evolution and a foundation for genetic interactions that shape phenotypic diversity. Compensation is a major form of paralog interaction, but how compensation relationships change as allelic variation accumulates is unknown. Here, we leveraged genomics and genome editing across the Solanaceae family to capture the evolution of compensating paralogs. Mutations in the stem cell regulator CLV3 cause floral organs to overproliferate in many plants. In tomato, this phenotype is partially suppressed by transcriptional upregulation of a closely related paralog. Tobacco lost this paralog, resulting in no compensation and extreme clv3 phenotypes. Strikingly, the paralogs of petunia and groundcherry nearly completely suppress clv3, indicating a potent ancestral state of compensation. Cross-species transgenic complementation analyses show this potent compensation partially degenerated in tomato due to a single amino acid change in the paralog and cis-regulatory variation that limits its transcriptional upregulation. Our findings show how genetic interactions are remodeled following duplications, and suggest that dynamic paralog evolution is widespread over short time scales and impacts phenotypic variation from natural and engineered mutations.