A map of rice genome variation reveals the origin of cultivated rice

Abstract

Crop domestications are long-term selection experiments that have greatly advanced human civilization. The domestication of cultivated rice (Oryza sativa L.) ranks as one of the most important developments in history. However, its origins and domestication processes are controversial and have long been debated. Here we generate genome sequences from 446 geographically diverse accessions of the wild rice species Oryza rufipogon, the immediate ancestral progenitor of cultivated rice, and from 1,083 cultivated indica and japonica varieties to construct a comprehensive map of rice genome variation. In the search for signatures of selection, we identify 55 selective sweeps that have occurred during domestication. In-depth analyses of the domestication sweeps and genome-wide patterns reveal that Oryza sativa japonica rice was first domesticated from a specific population of O. rufipogon around the middle area of the Pearl River in southern China, and that Oryza sativa indica rice was subsequently developed from crosses between japonica rice and local wild rice as the initial cultivars spread into South East and South Asia. The domestication-associated traits are analysed through high-resolution genetic mapping. This study provides an important resource for rice breeding and an effective genomics approach for crop domestication research.

Figure 1. Genetic structure and association analysis in the wild rice population.

a, Neighbour-joining tree of 446 O. rufipogon accessions, which was calculated from ∼5 million SNPs, identifies the three groups of Or-I (red), Or-II (grey) and Or-III (blue). b, Geographic origins of wild rice accessions. c, The level of genetic differentiation (F_ST) in O. rufipogon population around the DPL2 gene that underlies indica–japonica hybrid incompatibility in rice. d, Regional Manhattan plots of GWAS for tiller angle in O. rufipogon population identify a known gene, PROG1, using a compressed mixed linear model. The genome-wide significance threshold (1 × 10⁻⁶) and the position of the peak SNP are indicated by a horizontal dash-dot line and a vertical red line, respectively. PowerPoint slide

Figure 2. Genome-wide relationship between cultivated rice and its wild progenitor.

a, Phylogenetic tree of the full population (446 O. rufipogon accessions and 1,083 O. sativa varieties) calculated from ∼8 million SNPs in O. rufipogon and O. sativa. The double-layer rings indicate O. rufipogon (outer ring: Or-I, Or-II and Or-III are coloured in red, grey and blue, respectively) and O. sativa (inner ring: indica and japonica subspecies are in pink and sky blue, respectively). b, Illustration of genetic diversity and population differentiation in O. rufipogon and O. sativa. The size of the circles represents the level of genetic diversity (π) of the groups, and the F_ST values between the groups are indicated. ind, indica; jap, japonica. c, The spectrum of allele frequencies at the causal polymorphisms of Ghd7, DPL2 and GS3. PowerPoint slide

Figure 3. Whole-genome screening and functional annotations of domestication sweeps.

a, Whole-genome screening of domestication sweeps in the full population of O. rufipogon and O. sativa. The values of π_w/π_c are plotted against the position on each chromosome. The horizontal dashed line indicates the genome-wide threshold of selection signals (π_w/π_c > 3). b–d, A large-scale high-resolution mapping for fifteen domestication-related traits was performed in an O. rufipogon × O. sativa population. The domestication sweeps overlapped with characterized domestication-related QTLs are shown in dark red, and the loci with known causal genes are shown in red. Among them, three strong selective sweeps were found to be associated with grain width (b), grain weight (c) and exserted stigma (d), respectively. In b–d, the likelihood of odds (LOD) values from the composite interval mapping method are plotted against position on the rice chromosomes. Grey horizontal dashed line indicates the threshold (LOD > 3.5). PowerPoint slide

Figure 4. Genetic and geographic origins of rice domestication.

a, Phylogenetic tree of 446 O. rufipogon accessions and 1,083 O. sativa varieties calculated from SNPs in the overall regions of the 55 major domestication sweeps. b, Geographic locations of 62 O. rufipogon accessions, whose phylogenetic positions during domestication are indicated. Colour index represents the average of the genetic distance of O. rufipogon accessions to all cultivated rice accessions. Two major rivers in southern China are labelled in grey in the map. c, The average distance of O. rufipogon accessions from different countries to all cultivars. The distance was estimated by simple matching distance of SNPs around the Bh4 locus or all SNPs within the 55 domestication sweeps. d, The average distance of O. rufipogon accessions from different provinces in southern China to all cultivars. e, Schematics of the origin of cultivated rice. The aus and aromatic rice are minor groups of rice accessions with small geographic distributions. PowerPoint slide