Wheat Topoisomerase VI Positively Regulates the Biosynthesis of Cuticular Wax and Cutin

Lipophilic cuticles mainly composed of wax mixtures and cutin matrices seal the plant epidermis and control plant development and environmental adaptation. Although cuticle-associated traits have been selected in the breeding of agronomically important cereal bread wheat, the biosynthesis of wheat cuticular wax and cutin remains poorly understood. Herein, wheat topoisomerase VI was characterized as an essential activator of cuticular wax and cutin biosynthesis. Knock-down of wheat TaTOP6A, TaTOP6B, TaRHL1, or TaBIN4 gene encoding component of topoisomerase VI resulted in decreased loads of leaf cuticular wax and cutin, as well as increased leaf cuticle permeability. Moreover, TaCYP86A2 was identified as a key component of the wheat cutin biosynthetic machinery. Reduction of wheat TaCYP86A2 expression led to decreased cutin accumulation and enhanced cuticle permeability. In addition, TaTOP6A, TaTOP6B, TaRHL1, or TaBIN4 was shown to enrich at the promoter regions of the wax biosynthesis gene TaKCS1 and the cutin biosynthesis gene TaCYP86A2. Importantly, chromatin at TaKCS1 and TaCYP86A2 promoters is marked by high nucleosome occupancy and low histone acetylation in TaTOP6A-, TaTOP6B-, TaRHL1-, or TaBIN4-silenced wheat leaves. These results collectively support that wheat topoisomerase VI positively regulates the biosynthesis of cuticular wax and cutin probably via maintaining a permissive chromatin state at TaKCS1 and TaCYP86A2 genes.