Transcriptomic network analyses shed light on the regulation of cuticle development in maize leaves

Significance Plant cuticles provide barriers to water loss and arose as aquatic plants adapted to the dry terrestrial environment. The cuticle components, waxes and the fatty acid-based polymer cutin, are synthesized in the plant epidermis, exported across the cell wall, and deposited on the plant surface. This study suggests a role for PHYTOCHROME light receptors during cuticle development in leaves of maize and moss, diverse species that are separated by more than 400 million y of land plant evolution. We hypothesize that phytochrome-mediated light signaling contributed to the evolution of cuticles in land plants.
Plant cuticles are composed of wax and cutin and evolved in the land plants as a hydrophobic boundary that reduces water loss from the plant epidermis. The expanding maize adult leaf displays a dynamic, proximodistal gradient of cuticle development, from the leaf base to the tip. Laser microdissection RNA Sequencing (LM-RNAseq) was performed along this proximodistal gradient, and complementary network analyses identified potential regulators of cuticle biosynthesis and deposition. A weighted gene coexpression network (WGCN) analysis suggested a previously undescribed function for PHYTOCHROME-mediated light signaling during the regulation of cuticular wax deposition. Genetic analyses reveal that phyB1 phyB2 double mutants of maize exhibit abnormal cuticle composition, supporting the predictions of our coexpression analysis. Reverse genetic analyses also show that phy mutants of the moss Physcomitrella patens exhibit abnormal cuticle composition, suggesting an ancestral role for PHYTOCHROME-mediated, light-stimulated regulation of cuticle development during plant evolution.