Peroxisomal CuAO zeta and its product H2O2 regulate the distribution of auxin and IBA-dependent lateral root development in Arabidopsis

Root system architecture depends on endogenous and environmental signals, including polar transport of the phytohormone auxin, reactive oxygen species (ROS), nutrient availability, and stresses. In our study, we describe a novel Arabidopsis thaliana peroxisome-localized copper amine oxidase zeta (CuAO zeta), which is highly expressed in cortical cells, and the ROS derived from CuAO zeta are essential for lateral root (LR) development. Loss of CuAO zeta results in retarded auxin-induced ROS generation, PINFORMED2 (PIN2)-mediated auxin transport, and LR development in response to added indole-3-butyric acid. Auxins enhance CuAO zeta protein levels and their cellular translocation toward the plasma membrane in the cortex. CuAO zeta interacts physically with PEROXINS5 via an N-terminal signal tag, Ser-Lys-Leu, and is transported into the peroxisome upon this interaction, which is required for the functions of CuAO zeta in the auxin response. Together, our results suggest a peroxisomal ROS-based auxin signaling pathway involving spatiotemporal-dependent CuAO zeta functional regulation of PIN2 homeostasis, auxin distribution, and LR development.