Light-triggered ROS signaling regulates abaxial cuticle permeability in developing duckweed fronds

Abstract The cuticle is an ancient innovation that enabled plants to colonize land by providing a protective yet selectively permeable barrier. Although its composition is well characterized, the developmental and environmental regulation of cuticle permeability remains unclear. Here, we used duckweed, a tiny aquatic plant that absorbs nutrients through a permeable abaxial frond surface, as a model to investigate the formation of water-permeable cuticles. During frond development, the abaxial surface gradually acquires permeability upon the emergence of the maternal pouch. Structural and biochemical analyses showed that this permeable cuticle is thinner, less compact, and depleted of very-long-chain alkanes compared to the adaxial surface. Transcriptomic profiling revealed the distal enrichment of light-responsive and cuticle-modifying genes, suggesting light-regulated cuticle remodeling. Consistent with this, light, rather than direct water contact, served as the key external cue; exposure of daughter fronds to unfiltered light without overlying tissue enhanced permeability, whereas a reduced red-to-far-red ratio attenuated it. This transition required the accumulation of reactive oxygen species in the abaxial epidermis, as inhibition of reactive oxygen species production suppressed permeable cuticle formation. Together, these findings show that duckweeds co-opt a light-quality sensing mechanism, reminiscent of terrestrial shade-avoidance signaling, to regulate reactive oxygen species-mediated cuticle permeability, revealing how developmental programs and environmental cues integrate to dynamically remodel cuticle properties in aquatic plants.