ENHANCER OF SHOOT REGENERATION 1 (ESR1) functions in trichome initiation in cucumber (Cucumis sativus L.)

Trichomes are crucial for plant resistance to biotic and abiotic stresses. In cucumber, the density and morphology of fruit spines directly influence fruit appearance and market value, making them a key agronomic trait. Nevertheless, the genetic regulators governing trichome initiation and development remain poorly understood. In this study, the AP2/ERF transcription factor ENHANCER OF SHOOT REGENERATION 1 (CsESR1) was identified and shown to be predominantly expressed in the epidermis of stems, leaves, flower buds, and ovaries, as confirmed by quantitative reverse transcriptase-polymerase chain reaction and GUS staining analyses. CRISPR/Cas9-mediated knockout of CsESR1 resulted in a marked decrease in spine density, altered spine morphology, and a glabrous phenotype in vegetative tissues including stems, leaves, and tendrils. Furthermore, the defective development of bloom trichomes in the Csesr1 mutant resulted in increased glossiness of the fruit peel. Protein interaction assays revealed that CsESR1 physically associates with key trichome regulators, CsTOE3, CsGL1, and CsTRY. Moreover, Csesr1 plants exhibited reduced aphid resistance, concomitant with altered expression of defense-related genes, phytohormone levels, and antioxidant enzyme activities. Collectively, this study establishes CsESR1 as a key regulator of trichome formation in cucumber and uncovers its role in plant defense, providing novel insights into the molecular networks coordinating epidermal differentiation and stress adaptation.