Identification of the Gene Controlling g-Decalactone Content in Strawberry Fruit Using Two Independent Genetic and Genomic Approaches

Understanding the basis for volatile organic compound (VOC) biosynthesis and regulation is of great importance for the genetic improvement of fruit flavor. Lactones constitute an essential group of fatty acid-derived VOCs conferring peach-like aroma to a number of fruits including peach, plum, pineapple and strawberry. Early studies on lactone biosynthesis suggest that several enzymatic pathways could be responsible for the diversity of lactones, but detailed information on them remained elusive. The content of g-decalactone is controlled by one dominant locus mapped to the bottom arm of LG III-2 in strawberry. Our laboratories unknowingly took separate yet complementary genomics approaches to simultaneously identify the fatty acid desaturase FaFAD1 as the gene underlying the locus that controls g-decalactone production in ripening fruits. The gene was discovered using genetic mapping, GC/MS and genome-wide transcriptome analysis using either in vivo or in silico bulked RNAseq expression data. The FaFAD1 gene is specifically expressed in ripe fruits and its expression fully correlates with the presence of g-decalactone in all 95 individuals of one of the mapping populations. A functional, PCR‐based molecular marker was developed that cosegregates perfectly with the phenotype in other F1 and BC1 populations. The marker also accurately predicted the volatile phenotype in germplasm outside our populations including cultivars and wild Fragaria species. Additional candidate genes of the biosynthetic pathway of lactones are also reported based on eQTL analysis. All together, these studies provide mechanistic information of how the production of g-decalactone is naturally controlled in strawberry, propose enzymatic activities necessary for the formation of this VOC in plants and deliver molecular markers that could be used for the selection of flavorful plants across the Rosaceae.