WOX1 controls leaf serration development via temporally restricting BRASSINAZOLE RESISTANT 1 and CUP SHAPED COTYLEDON 3 expression in Arabidopsis

Leaves have evolved shape diversity, ranging from simple leaves with a smooth margin to complicated shapes with toothed/serrated, lobed, and dissected leaves with leaflets. In the model plant Arabidopsis thaliana with simple leaves producing a serrated margin, boundary regulatory factor genes CUP SHAPED COTYLEDON 2 (CUC2) and CUC3 play important roles in promoting leaf initiation and maintenance of serration. Stem cell-related WUSCHEL-RELATED HOMEOBOX1 (WOX1) and PRESSED FLOWER (PRS)/WOX3 are also essential for leaf margin morphogenesis, but the role of WOX1 and PRS as well as the relationships between CUCs and WOXs for tooth development are unclear. In this study, we found that WOX1, but not PRS, prevents overproduction of number of teeth and excessive tooth size by limiting CUC3 expression to a moderate level in a temporally regulated manner. We also revealed that BRASSINAZOLE RESISTANT 1 (BZR1), a known regulator of plant development including boundary regions, is involved in WOX1 negative regulation of tooth development by repressing CUC3 expression during the initiation/early stage of tooth development. WOX1 parallelly limits BZR1 and CUC3 expression from the late stage of the first two teeth, while it restricts CUC3 activity in a BZR1-dependent manner from the initiation/early stage of subsequently developed teeth. This study uncovers a new mechanism for WOX1 in fine-tuning the leaf margin geometry.