A novel allele of Sh1 underlines the conversion of waxy corn to wx-sweet corn

Waxy corn and sweet corn represent the two major types of fresh-eating corn. Each has significant market value due to its unique sensory and nutritional profiles. Developing a novel variety that combines disirable traits of both would satisfy growing consumer demands and create new commercial opportunities. Here, from a fast neutron-mutagenized population of the waxy corn inbred line HB522, we identified a mutant named wx-sweet. Its kernels exhibit a combination of waxy texture and sweet flavor properties at filling stage. Using bulked segregant analysis (BSA) and fine mapping, we mapped the causal locus to SHRUNKEN1 (Sh1) on chromosome 9, which was validated by an allelic test using a known Mu-insertion mutant. Further sequencing analysis revealed a sequence disruption in the second exon of the Sh1 gene in wx-sweet, leading to loss of gene function. The study revealed that the novel allele of sh1 impaired sucrose synthase activity, resulting in a significant increase in soluble sugar content in the endosperm of wx-sweet kernels. Transcriptome analysis of wx and wx-sweet endosperms at various developmental stages indicated that the malfunction of Sh1 leads to altered expression of genes predominantly enriched in carbohydrate metabolism pathways. Moreover, metabolomic profiling showed an increased accumulation of both sucrose and raffinose, suggesting a profound shift in carbohydrate pathway. This metabolic signature likely contributes to the desirable sweet-waxy phenotype. Furthermore, we developed a molecular marker targeting the novel sh1 allele, providing an efficient tool for selecting sweet-waxy corn. In summary, this work not only provides a valuable genetic resource for sweet-waxy corn breeding but offers molecular insights into the metabolic bases underlying the combination of waxy and sweet traits.