ZmMS1 coordinates ROS homeostasis, lipid allocation, and male fertility for maize breeding applications

Identifying male-sterile genes and developing biotechnology-based male-sterility systems are crucial for advancing hybrid maize breeding. However, this progress is hampered by the limited number of characterized key regulators and their incomplete mechanistic understanding in male sterility, as well as fertility instability of male-sterile lines and a lack of efficient maintainer lines in maize. Here, we elucidate the multifaceted roles of ZmMS1, an LBD transcription repressor. ZmMS1 coordinates timely tapetal PCD by repressing ROS-scavenging genes to regulate anther ROS homeostasis, while its DNA-binding activity is redox-sensitive, suggesting a potential redox-dependent feedback mechanism. In addition, ZmMS1 balances lipid allocation between anther cuticle and pollen exine by directly repressing sporopollenin biosynthesis and indirectly promoting cutin/wax formation. Constitutive overexpression of ZmMs1 induces dwarfism associated with GA and ABA homeostasis, and produces ~50% sterile and small pollen grains in maize and rice, offering a potential route for dwarf and male-sterile breeding. Leveraging the findings that loss and precocious expression of ZmMs1 cause recessive and dominant sterility, respectively, we develop a non-transgenic multi-control sterility system and a dominant genic male-sterility system, both showing stable and complete sterility across diverse backgrounds without yield penalty, thereby providing flexible options for hybrid maize breeding. Our findings reveal that ZmMS1, as a redox-sensitive transcription factor, regulates male fertility with previously unrevealed mechanisms, and provide practical tools for efficient hybrid maize breeding.