Early Domestication History of Asian Rice Revealed by Mutations and Genome-Wide Analysis of Gene Genealogies

BACKGROUND: Asian rice (Oryza sativa L.) has been a model plant but its cultivation history is inadequately understood, and its origin still under debate. Several enigmas remain, including how this annual crop shifted its growth habit from its perennial ancestor, O. rufipogon, why genetic divergence between indica and japonica appears older than the history of human domestication, and why some domestication genes do not show signals of introgression between subgroups. Addressing these issues may benefit both basic research and rice breeding. RESULTS: Gene genealogy-based mutation (GGM) analysis shows that history of Asian rice is divided into two phases (Phase I and II) of about equal lengths. Mutations occurred earlier than the partition of indica and japonica to Os genome mark Phase-I period. We diagnosed 91 such mutations among 101 genes sampled across 12 chromosomes of Asian rice and its wild relatives. Positive selection, detected more at 5′ regions than at coding regions of some of the genes, involved 22 loci (e.g., An-1, SH4, Rc, Hd3a, GL3.2, OsMYB3, OsDFR, and OsMYB15), which affected traits from easy harvesting, grain color, flowering time, productivity, to likely taste and tolerance. Phase-I mutations of OsMYB3, OsHd3a and OsDFR were experimentally tested and all caused enhanced functions of the genes in vivo. Phase-II period features separate cultivations, lineage-specific selection, and expanded domestication to more genes. Further genomic analysis, along with phenotypic comparisons, indicates that O. sativa is hybrid progeny of O. rufipogon and O. nivara, inherited slightly more genes of O. rufipogon. Congruently, modern alleles of the sampled genes are approximately 6% ancient, 38% uni-specific, 40% bi-specific (mixed), and 15% new after accumulating significant mutations. Results of sequencing surveys across modern cultivars/landraces indicate locus-specific usages of various alleles while confirming the associated mutations. CONCLUSIONS: Asian rice was initially domesticated as one crop and later separate selection mediated by human resulted in its major subgroups. This history and the hybrid origin well explain previous puzzles. Positive selection, particularly in 5′ regions, was the major force underlying trait domestication. Locus-specific domestication can be characterized and the result may facilitate breeders in developing better rice varieties in future. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12284-022-00556-6.