Molecular Dosage Effect Reveals Semi-Dominant Maturation Underlying Single-Gene Heterosis in Tomato

The genetic basis of heterosis remains a contentious topic in plant genetics and crop improvement. Besides the widely accepted dominance complementation model, the disputed model of overdominance has received less attention. We have discovered cases of heterosis due to single gene heterozygosity in tomato, involving crosses between mutants and their isogenic progenitors. The higher yields observed in the single gene heterozygotes derive from mutations in a gene that modulate reproductive transitions and shoot architecture. We find that having only one functional copy of SINGLE FLOWER TRUSS (SFT) gives rise to more inflorescences, flowers and fruits. By dissecting the modular developmental growth habit of tomato, we support a model for heterosis centered on dosage effects involving genes with strong pleiotropic impacts on growth and development, altering the dosage of a single gene due to mutant heterozygosity impacts multiple component traits leading to cumulative overdominance. To test this hypothesis, we profiled genome-wide gene expression in expanding leaves and developing meristems by mRNA-Seq at precise stages of development from wild type, SFT mutants, and hybrid plants. In sft/+ plants, molecular dosage effects cause intermediate tissue maturation, slight delay in progression to flowering and sympodial termination, a semi-dominant phenotype. Together, our findings suggest that local dosage effects in different tissue types are rapidly amplified due to the tight gene regulatory networks in which these genes reside. Thus, we advance a framework for further exploration of single gene overdominance in which local dosage effect of strongly pleiotropic loci progress gradually into global heterotic effects.