CsMYB36-mediated ROS homeostasis modulates the switch from cell division to differentiation in cucumber glandular trichome.

Glandular trichomes (GTs) synthesize, store, and secrete diverse specialized metabolites that protect plants against biotic and abiotic stress. The bloom is deposited on the GTs and is perceptible on the surface of the cucumber fruit. Our previous investigation revealed the absence of bloom on the fruit surface in the loss-of-function CsMYB36 plants. GTs are formed through a series of cell differentiation events that support compound production. However, the mechanisms governing these events remain unclear. Here, we found GT cells initiate excessive periclinal divisions and fail to differentiate into functional GT cells in the absence of CsMYB36 based on the establishment of a detailed developmental process of GT in cucumber. We further found that CsMYB36 and CsGL1 form a positive feedback loop to regulate the cell differentiation of GT. DNA affinity purification (DAP)-seq, combined with RNA-seq data demonstrated that CsMYB36/CsGL1 can regulate the expression of phenylalanine synthesis-related genes, including peroxidase 53 (CsPRX53) which is a reactive oxygen species (ROS)-scavenging enzyme. H2O2 effectively inhibited GT cell division in Csmyb36 mutant plants. Collectively, our findings demonstrate that CsMYB36 combined with CsGL1 balances cell division and differentiation in the GT by mediating ROS homeostasis, thus affecting bloom production in cucumbers.