Abstract

The orchestration of source, flow, and sink is fundamental to efficient grain filling in maize, yet the regulatory network synchronizing these processes remains enigmatic. To identify key regulators, we used the sucrose transporter ZmSUT1, a critical component for phloem loading and unloading, as a molecular target. This approach showed that the bZIP transcription factor ZmbZIP39 acts as a central coordinator of grain filling, regulating photosynthesis (source), sucrose transport (flow), and sucrose metabolism and nutrient storage (sink). Mechanistically, ZmbZIP39 directly activates the expression of ZmSUT1 and ZmSUT7, facilitating sucrose loading and long-distance transport from leaves to developing kernels. It also promotes sucrose cleavage by directly upregulating three sucrose synthase-encoding genes. Furthermore, ZmbZIP39 directly controls the expression of the zein-encoding genes and endosperm-filling hub Opaque2, thereby driving nutrient storage and endosperm development. ZmbZIP39 also functions within a higher-order regulatory complex, synergizing with key factors such as ZmABI19, ZmbZIP29, OHP1, OHP2, and ZmNAC130. ZmbZIP39 autoactivation activity creates a positive feedback loop that strengthens its downstream network. Our findings establish ZmbZIP39 as a central coordinator of source-flow-sink relations.