The trade-off mechanism between fiber elongation and seed vigor formation mediated by the RCD1-MYC3 module in cotton.

Cotton fiber length and seed vigor are crucial traits determining cotton farming efficiency and commercial value. Cotton fiber elongation and seed vigor establishment exhibit high spatiotemporal overlap and a close relationship. However, the underlying regulatory mechanisms orchestrating these two developmental processes remain poorly understood. Here, we identified an antagonistic module comprising radical-induced cell death 1 protein (GhRCD1) and transcription factor GhMYC3, which participates in this synergistic development. GhRCD1 positively regulated fiber elongation but negatively regulated seed vigor, whereas GhMYC3 had the opposite effects. Further studies demonstrated that GhRCD1 interacted with GhMYC3 through its RST domain, thereby attenuating GhMYC3-mediated promoter binding and transcriptional repression of GhGPX4, GhPER25, GhPER63, GhKCS12, GhCUT1, and GhFAD7A-1. In elongating fibers, higher GhRCD1 levels and lower GhMYC3 levels activate this module, which attenuates reactive oxygen species (ROS) signaling and increases linolenic acid and very-long-chain fatty acid (VLCFA) levels, thereby promoting fiber elongation. In ripening seeds, lower GhRCD1 and higher GhMYC3 repress this module, which inhibits peroxidase (PER)-mediated ROS-cell wall demethylesterification-seed mechanical properties pathway, thus contributing to seed vigor formation. The genetic evidence further supported the GhMYC3 epistasis effect on GhRCD1 during fiber elongation and seed maturation coordination. Together, our findings elucidate a trade-off mechanism orchestrated by the antagonistic GhRCD1-GhMYC3 module, which coordinates cotton fiber elongation and seed vigor formation through their specific expression profiles and downstream regulatory networks in developing fibers and seeds. This study provides a basis for synergistic improvement of cottonseed and fiber quality.