Fruit skin netting in cucumber (Cucumis sativus) is associated with important fruit quality attributes. Two simply inherited genes H (Heavy netting) and Rs (Russet skin) control skin netting, but their molecular basis is unknown. Here, we reported map-based cloning and functional characterization of the candidate gene for the Rs locus that encodes CsSHINE1 (CsSHN1), an AP2 domain containing ethylene-responsive transcription factor protein. Comparative phenotypic analysis in near-isogenic lines revealed that fruit with netted skin had different epidermal structures from that with smooth skin including thicker cuticles, smaller, palisade-shaped epidermal and sub-epidermal cells with heavily suberized and lignified cell walls, higher peroxidase activities, which suggests multiple functions of CsSHN1 in regulating fruit skin netting and epidermal cell patterning. Among three representative cucumber inbred lines, three haplotypes at three polymorphic sites were identified inside CsSHN1: a functional copy in Gy14 (wild type) with light fruit skin netting, a copy number variant with two tandemly arrayed functional copies in WI7120 with heavy skin netting, and a loss-of-function copy in 9930 with smooth skin. The expression level of CsSHN1 in fruit exocarp of three lines was positively correlated with the skin netting intensity. Comparative analysis between cucumber and melon revealed conserved and divergent genetic mechanisms underlying fruit skin netting/reticulation that may reflect the different selection histories in the two crops. A discussion was made on genetic basis of fruit skin netting in the context of natural and artificial selections of fruit quality-related epidermal features during cucumber breeding.
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