A 48 kb fragment deletion is required for the formation of trichomes in watermelon

• The cause of the formation of the glabrous mutant in watermelon was identified. • Three molecular markers cosegregated associated with the glabrous trait of watermelon were developed. • Differentially expressed genes affecting trichome development were identified. • Genes associated with the development of trichomes in watermelon were identified by WGCNA. Trichomes, subsidiary structures of the plant epidermis, are widely distributed in the epidermal tissue of the aerial part of the plant. Research on the molecular mechanism of multicellular trichomes is in the early stages, focusing mainly on cucumber, tomato and cotton, and research on the genetic control and regulation of watermelon ( Citrullus lanatus ) trichome development is still lacking. In the present study, we identified a watermelon fertile glabrous mutant, WMX, which was completely glabrous during development. Genetic analysis suggested that a single recessive gene controls the glabrous phenotype. Genome resequencing and genome-wide association analysis of parents and F 2 populations revealed that a large-fragment deletion of nearly 48 kb on chromosome 8 of watermelon, including 10 predicted genes, was required for trichome formation in watermelon. PCR-based markers were developed to represent the large-fragment deletion, and they cosegregated in the F 2 and BC 1 F 1 populations, suggesting that this deletion is the cause of glabrous-mutant formation in watermelon. Weighted correlation network analysis revealed one coexpression module, which contained 219 genes, highly associated with the glabrous phenotype. Among the 77 differentially expressed genes in the coexpression module associated with the glabrous phenotype, six were in the large-fragment deletion, and nine were associated with trichome development. Notably, only Cla97C08G161400 in the large-fragment deletion was associated with trichome development and was the most critical potential candidate gene for regulating trichome development in watermelon. The results of this study provide insights into the causes of glabrous mutant formation, which will contribute to a better understanding of the genetic control of trichome development in watermelon and marker-assisted selection of new watermelon varieties.