Cucumis fruit surface biology: Genetic analysis of fruit exocarp features in melon (C. melo) and cucumber (C. sativus)
Authors: Grumet R. , Burger J. , Tadmor Y. , Gur A. , Barry C. , Schäffer A. , Petreikov M. ,   Michigan State University,   United States-Israel Binational Agricultural Research and Development Fund
Published: October 2023

The fruit surface (exocarp) is a unique tissue with multiple roles influencing fruit growth and development, disease susceptibility, crop yield, post-harvest treatments, shipping and storage quality, and food safety. Furthermore, highly visible exocarp traits are the consumer's first exposure to the fruit, serving to identify fruit type, variety, attractiveness, and market value. Cucurbit fruit, including the closely related Cucumis species, melon (C. melo) and cucumber (C. sativus), exhibit tremendous diversity for fruit surface properties that are not present in model species. In this project, we identified genetic factors influencing Cucumis fruit surface morphology with respect to important quality determinants such as exocarp and flesh color, cuticle deposition, and surface netting. We employed a combination of approaches including: genome-wide association studies (GWAS) utilizing an extensive melon population and the U.S. Plant Introduction (PI) collection for cucumber to identify genomic regions associated with natural variation in fruit surface traits; bulked segregant RNA-seq (BSR-seq) analysis of bi-parental F2:3 or RIL (recombinant inbred line) populations to genomic regions and candidate genes segregating for fruit surface traits; and comparison of syntenic genomic regions and identification of homologous candidate genes. Candidate genes were examined for sequence and/or expression differences during fruit development that correspond with phenotypic differences. Primary outcomes of the work included identification of candidate genes influencing cuticle deposition, epidermal cell structure, surface netting, and intensity of rind and flesh color. Parallel studies identified mutations within the cucumber and melon homologs of the transcription factor WIN1 (WAX INDUCER1) as a significant factor influencing these surface properties. Additional QTL (quantitative trait loci) were identified in both species, and candidate genes in melon include a novel beta-glucosidase involved in lignin production and an integral membrane protein potentially involved in cuticle metabolism. Genetic resources and biochemical approaches have been developed to study cuticle and wax deposition in both species: segregating populations of melon were developed and sequenced for bulked segregant analysis and samples collected for metabolic analysis; an isolation procedure was developed for lipid droplets from cucumber peel and metabolomic analyses have been initiated. Genetic studies in melon identified mutations in a candidate gene (APRR2), associated with light immature rind, and further indicated that this gene is also associated with color intensity of both mature rinds and flesh, making it a good target for breeding. GWAS studies utilizing the cucumber core diversity population are being performed to identify additional sources of variation for fruit surface properties, map QTL, and examine for synteny with melon. Collectively these studies identified genetic regions associated with important quality traits and contributed to our understanding of underlying biological processes associated with fruit surface development. Knowledge of genetic control of these characteristics can facilitate more efficient breeding for important fruit surface traits.