A GRX-SOD module maintains superoxide homeostasis and meristem development in maize

The continuous initiation of plant aerial organs relies on the maintenance of dynamic stem cell homeostasis within the shoot apical meristem (SAM). Although reactive oxygen species (ROS) have emerged as crucial signals determining cell fate, how plants precisely maintain SAM-specific ROS homeostasis remains to be elucidated. Here, we report that a redox regulatory module comprising the maize CC-type glutaredoxin MSCA1 and its homologs regulates meristem architecture by maintaining superoxide homeostasis in the SAM. We found that the superoxide anion (O₂^•-) is specifically enriched in the central zone of the maize SAM, whereas the loss of the GRX module leads to strikingly decreased O₂^•- accumulation, resulting in SAM size reduction and impaired leaf formation. MSCA1 physically interacts with the superoxide dismutase ZmCSD5, and loss of GRX function is associated with elevated total SOD activity, supporting a working model in which MSCA1 may restrain ZmCSD5-associated SOD activity and thereby limit excessive O₂^•- scavenging in the SAM. Furthermore, loss-of-function zmcsd5 mutants exhibit a significantly enlarged SAM, genetically supporting the proposed MSCA1-ZmCSD5 regulatory module. Our findings reveal how superoxide homeostasis is precisely maintained in the SAM to control development, providing potential genetic targets for the molecular improvement of crop architecture and yield traits.