Natural variant of microProtein SMART1 confers 3S plant architecture traits and high-density tolerance in maize

Abstract High-density planting is a critical strategy for maximizing maize (Zea mays L.) yield. The ideotype for maize dense planting requires shade-tolerant traits characterized by semi-dwarf, sturdy stems, and smart-canopy structure (termed 3S traits), which collectively enhance lodging resistance and light capture efficiency. However, the genetic basis of these 3S traits regulation in maize remains unclear. Here, we identify Shade-responsive MicroProtein Architecture Remodeling Target 1 (SMART1) as a pivotal regulator that enhances 3S traits, manifesting as semi-dwarf plant height, robust stems and upright upper leaves. Field trials demonstrate that SMART1 overexpression significantly improves density tolerance, photosynthetic capacity and grain yield. Association analysis revealed that natural variations in SMART1 influence its binding affinity to a phytochrome-interacting factor, ZmPIF5.2, thereby modulating its allosteric deactivation. These molecular interactions subsequently repress the expression of ZmMYBs, ZmCRRs, and ZmCYPs genes, contributing to phenotypic variation in shade-related traits across maize inbred lines and haplotype-specific overexpression lines. Evolutionary analysis further reveals that the shade-tolerant haplotype SMART1Hap2 underwent positive selection during maize domestication and modern breeding. Our findings identify SMART1 as a key regulator of 3S traits under normal and high-density conditions and provide a promising genetic target for breeding maize varieties with enhanced density tolerance.