Multi-omics landscapes reveal the genetic basis of graft compatibility in tomato

Abstract Grafting is a horticultural strategy for improving crop productivity and tolerance to biotic and abiotic stresses. However, the genetic basis of graft compatibility and its effects on plant growth and fruit metabolism remain poorly understood in tomato. In this study, we systematically evaluated the growth and development of tomato ( Solanum lycopersicum L.) of scions ‘72–69’ grafted onto 14 rootstocks (9 novel F 1 hybrids [GC1–GC9] and 5 commercial cultivars [GC10–GC14]). Based on mature-stage growth and yield performance, the 14 graft combinations were classified into high-compatibility (high-com, GC1–GC5) and low-compatibility (low-com, GC6–GC14) groups. Low-com combinations exhibited reduced vegetative growth and yield, earlier fruit maturation, and structural abnormalities in the scion stem tissues, whereas high-com combinations maintained stronger growth and productivity. Comparative genomic analysis of F 1 rootstocks with contrasting compatibility phenotypes identified 28 candidate genomic regions encompassing 203 genes. Among these, ethylene-overproduction protein 1 ( SlETO1 ) and wall-associated kinase-like ( SlWAKL10 ) contained heterozygous coding variants within conserved domains in the low-com rootstocks, whereas the corresponding loci were homozygous in the high-com rootstocks, suggesting their potential association with graft compatibility. Integrated transcriptomic and metabolomic analyses revealed distinct molecular and metabolic responses between the two graft-compatibility groups. Low-com fruits exhibited enhanced expression of stress- and ethylene-related genes and accumulated substantially higher levels of soluble sugars, including glucose, fructose, and sucrose, whereas high-com fruits showed greater accumulation of organic acids. Correlation analyses further indicated associations between SlWAKL10 and SlETO1 expression and soluble sugar accumulation. Collectively, our work establishes a genetic framework for rootstock-scion compatibility and reveals its systemic effects on fruit metabolism, providing critical insights for molecular breeding of graft-compatible tomato rootstocks.