Abstract

Sexual reproduction, a nearly universal feature of eukaryotes, begins with the fertilization of gametes. Zoidogamy, or fertilization mediated by motile spermatozoids, represents an ancestral mode predating the evolution of pollen tube-based fertilization in angiosperms. This mode dominated a long span of evolutionary history and remains widespread among early-diverging plants and animals. However, the molecular mechanisms underlying this ancient fertilization process in plants remains poorly understood. In the liverwort Marchantia polymorpha , we identify a mechanism by which the peptide hormone MpRALF1 regulates sperm motility through reactive oxygen species (ROS). The sperm-derived MpRALF1 is perceived by a receptor complex composed of the MpFERONIA receptor kinase and its co-receptor MpLLG. This signalling module activates NADPH oxidase-mediated ROS production, thereby enhancing sperm velocity and progressive motility to ensure fertilization. Our study reveals the ancient origin of RALF peptide signalling in land plants and establishes ROS as a conserved mechanism governing sperm motility across kingdoms.