The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication

Abstract

The cultivation of rice in Africa dates back more than 3,000 years. Interestingly, African rice is not of the same origin as Asian rice (Oryza sativa L.) but rather is an entirely different species (i.e., Oryza glaberrima Steud.). Here we present a high-quality assembly and annotation of the O. glaberrima genome and detailed analyses of its evolutionary history of domestication and selection. Population genomics analyses of 20 O. glaberrima and 94 Oryza barthii accessions support the hypothesis that O. glaberrima was domesticated in a single region along the Niger river as opposed to noncentric domestication events across Africa. We detected evidence for artificial selection at a genome-wide scale, as well as with a set of O. glaberrima genes orthologous to O. sativa genes that are known to be associated with domestication, thus indicating convergent yet independent selection of a common set of genes during two geographically and culturally distinct domestication processes.

Figure 1. The O. glaberrima genome (CG14 v1).

Concentric circles show structural, functional and evolutionary aspects of the genome: A, chromosome number; B, heat map view of genes; C, repeat (RNA and DNA TEs without MITEs) density in 200-kb windows (red, average +1 s.d.; blue, average −1 s.d.; yellow, gene and repeat density between red and blue); and D paralogous relationships between O. glaberrima chromosomes.

Figure 2. Population structure analysis of 94 O. barthii accessions.

(a) Population structure of 94 O. barthii accessions inferred using ADMIXTURE. Each color represents one population. The length of each segment in each vertical bar represents the proportion contributed by ancestral populations. The O. barthii population is partitioned into four subgroups (OB-I, OB-II, OB-III and OB-V), as well as an admixed group (OB-IV). (b) PCA of 94 O. barthii accessions using all identified SNPs as markers. The O. barthii accessions from the same subgroup are clustered together. (c) NJ phylogenetic tree of 94 O. barthii accessions.

Figure 3. Identification of the domestication center of O. glaberrima.

(a) NJ phylogenetic tree of 20 O. glaberrima and 94 O. barthii accessions. All but one of the O. glaberrima accessions (black) are clustered with O. barthii accessions from group OB-V (green). (b) The proportion of each group of O. barthii accessions originating from different countries in Africa. All O. barthii accessions collected from the countries in the proposed domestication center (highlighted in black) are from the OB-V and OB-IV admixture groups. The proportion of O. barthii from the OB-V and OB-IV admixture groups found in each country decreased with distance from the domestication center, whereas the O. barthii accessions from other subgroups showed the opposite trend.

Figure 4. Identification of candidate regions of artificial selection during O. glaberrima domestication.

Plot of the composite likelihood ratio (CLR) across O. glaberrima genome. The red dashed line indicates the cutoff value for the 0.5% outlier regions with significant deviations from neutrality, indicating evidence of recent selective sweeps.

Figure 5. Sequence comparisons of OsSh1 and Sh4.

(a) Orthologous gene relationship of the OsSh1 region of O. sativa ssp. japonica (Os) with those of O. barthii (Ob) and O. glaberrima (Og). The 45-kb deletion (red triangle) resulted in the complete removal of the OsSh1 ortholog and three additional genes in O. glaberrima (red rectangle). Inversion is indicated with blue arrows. U and D represent upstream and downstream genes relative to OsSh1, respectively (U1, LOC_Os03g44680; U2, LOC_Os03g44690; OsSh1, LOC_Os03g44710; D1, LOC_Os03g44720; D2, LOC_Os03g44740; D3, LOC_Os03g44750; D4, LOC_Os03g44760; D5, LOC_Os03g44780). (b) Sequence comparison of Sh4 of O. sativa ssp. japonica and O. glaberrima. Two insertions (Ins) and three deletions (Del) of O. glaberrima compared to O. sativa ssp. japonica are shown as brown triangles and blue triangles, respectively. Ten SNPs are labeled a–j. The causative mutation (f) of the non-shattering phenotype in O. sativa is highlighted in red. This mutation did not exist in O. glaberrima.