Integrative multi-omics analysis reveals the domestication mechanism of black rice

Abstract Black rice, a nutritionally superior yet genetically uncharacterized germplasm, exhibits extreme rarity (∼ 1%) in natural rice populations. Here, we establish a global germplasm collection of 367 black rice accessions and employ integrated multi-omics (genomics, transcriptomics, metabolomics) to dissect its divergence from white rice. Population genomic analyses reveal a two-step domestication trajectory for black rice from wild progenitor: initial Rc-mediated loss of proanthocyanidin pigmentation, followed by OsKala4/OsMYB3-driven anthocyanin activation under artificial selection. Genome-wide scans identify 238 differentially selected regions between black and white rice that orchestrate extensive transcriptomic reprogramming (up to 22% differentially expressed genes) and metabolomic remodeling (up to 32% differentially accumulated metabolites) in black rice seeds. Multi-omics analysis and genome-wide association study uncover previously uncharacterized regulators (OsWRKY1, OsBBX13, OsTT12) that synergistically enhance the MBW transcriptional complex to regulate anthocyanin biosynthesis and vacuolar sequestration. Furthermore, we reconstructed a comprehensive biosynthetic pathway network for phenolic acids and flavonoids in black rice through integration of experimental metabolomic and transcriptomic datasets with KEGG pathway annotations. Finally, we evaluated the selection status of 225 quantitative trait genes and compared agronomic traits between black and white rice. Our findings provide a molecular roadmap for precision breeding strategies to develop elite black rice cultivars with optimized nutritional and agronomic performance.