The transcription factor ZmbZIP39 coordinately regulates both plant architecture and grain filling in maize

Efficient sucrose partitioning is a promising characteristic to improve crop yield, involving sucrose transport, sucrose metabolism, and sucrose utilization. However, it is still elusive how these processes are coordinately regulated to sustain a large amount of sucrose demands during grain filling. In this work, the classical sucrose transporter ZmSUT1 was used as an example to identify the potential upstream regulators, in which ZmSUT1 is crucial for plant architecture, efficient sucrose allocation, and yield improvement. The ubiquitously expressed transcription factor ZmbZIP39 was found to specifically and directly bound to the ZmSUT1 promoter and performed positive regulation. Mutation of ZmbZIP39 displayed dwarf plants with declined photosynthetic efficiency, advanced leaf senescence and sugar hyperaccumulation in leaves, leading to decreased kernel weight and nutrient storage, whereas the ZmbZIP39 overexpression lines performed the opposite roles. Global RNA-seq analysis revealed that ZmbZIP39 apparently influenced the biological processes, encompassing photosynthesis, phytohormone levels, cell cycle process, seed development, starch metabolic process, etc. Combination analysis of ChIP-seq and RNA-seq analysis identified 303 high-confidence targes regulated by ZmbZIP39. Notably, ZmbZIP39 directly regulated three sucrose synthase-encoding genes to increase sucrose synthase activity. ZmbZIP39 bound to the promoters of three zein-encoding genes and the endosperm-filling central regulator Opaque2 to promote nutrient storage accumulation. ZmbZIP39 also interacts with several key endosperm-filling regulators to synergistically promote endosperm-filling initiation and grain filling, encompassing OHPs, ZmNAC128, ZmNAC130, ZmABI19, and ZmbZIP29. Overall, this work demonstrates that three important traits-sucrose transport, sucrose metabolism, and sucrose utilization- are precisely regulated and associated by ZmbZIP39 to elaborately modulate plant architecture, efficiently enhance yield and nutrient reserve synthesis.