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. 2019 Mar 7;15(3):e1007414.
doi: 10.1371/journal.pgen.1007414. eCollection 2019 Mar.

The complex geography of domestication of the African rice Oryza glaberrima

Jae Young Choi  1 , Maricris Zaidem  1 , Rafal Gutaker  1 , Katherine Dorph  1 , Rakesh Kumar Singh  2 , Michael D Purugganan  1   3
Affiliations

The complex geography of domestication of the African rice Oryza glaberrima

Jae Young Choi et al. PLoS Genet. .

Abstract

While the domestication history of Asian rice has been extensively studied, details of the evolution of African rice remain elusive. The inner Niger delta has been suggested as the center of origin but molecular data to support this hypothesis is lacking. Here, we present a comprehensive analysis of the evolutionary and domestication history of African rice. By analyzing whole genome re-sequencing data from 282 individuals of domesticated African rice Oryza glaberrima and its progenitor O. barthii, we hypothesize a non-centric (i.e. multiregional) domestication origin for African rice. Our analyses showed genetic structure within O. glaberrima that has a geographical association. Furthermore, we have evidence that the previously hypothesized O. barthii progenitor populations in West Africa have evolutionary signatures similar to domesticated rice and carried causal domestication mutations, suggesting those progenitors were either mislabeled or may actually represent feral wild-domesticated hybrids. Phylogeographic analysis of genes involved in the core domestication process suggests that the origins of causal domestication mutations could be traced to wild progenitors in multiple different locations in West and Central Africa. In addition, measurements of panicle threshability, a key early domestication trait for seed shattering, were consistent with the gene phylogeographic results. We suggest seed non-shattering was selected from multiple genotypes, possibly arising from different geographical regions. Based on our evidence, O. glaberrima was not domesticated from a single centric location but was a result of diffuse process where multiple regions contributed key alleles for different domestication traits.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Geography of west Africa and approximate geographic regions involved in the O. glaberrima domestication model postulated by Portères [8,9].
Fig 2
Fig 2. Ancestry proportion estimates and their geographic distribution in O. glaberrima.
On the left panel shows ancestry proportions estimated from NGSadmix assuming K = 3, 5, 7, and 9. Black stars below the admixture barplot indicate O. glaberrima individuals. Colored stars above admixture barplot are the O. barthii grouping designated by Wang et al. [13] where blue: OB-I, brown: OB-II, red: OB-III, yellow: OB-IV, and pink: OB-V group. On the right panel shows the ancestry proportion of each individual and their geographical region.
Fig 3
Fig 3. Phylogenomic and principal component analysis of African rice.
(A) Neighbor-joining tree built using a distance matrix estimated from NGSdist. Color strips represent group of O. glaberrima individuals sharing a common ancestor. Internal branches with red circle denote bootstrap support of greater then 80%. Dark arrows indicates the O. glaberrima grouping with divergent O. barthii groups, and white arrows indicates the O. glaberrima grouping with OB-G group O. barthii. (B) Geographical distribution of each individual and colored by its grouping status as outlined in (A). (C) Principal component analysis conducted using NGScovar. Individuals are color coded according to (A).
Fig 4
Fig 4. Treemix admixture graph of genetic groups from O. barthii, O. glaberrima, and O. rufipogon.
Admixture graphs are shown for models assuming zero to two migration events. Numbers on nodes represent bootstrap support after 100 replicates. Residuals for each migration model are shown below the graph.
Fig 5
Fig 5. Evolutionary relationship between wild and domesticated African rice.
(A) Pairwise Fst values between O. glaberrima and O. barthii genetic groups. (B) Average linkage disequilibrium between pair of SNPs.
Fig 6
Fig 6
Haplotype analysis of the three domestication genes (A,D,G) PROG1, (B,E,H) sh4, and (C,F,I) sh1. Haplotype structures are shown for the genes (A) PROG1, (B) sh4, and (C) sh1. Homozygote genotype not identical to reference genome is shown in dark grey, heterozygote genotype shown in lighter shade of grey, and homozygote genotype identical to reference genome shown in lightest shade of grey. Regions are showing polymorphic sites from 25 kbp up- and downstream of the domestication gene. In sh4 (B) the position of the causal domestication mutation is shown in arrow and OG-A1 samples without the causal mutation are indicated with a star. In PROG1 (A) and sh1 (C) region upstream and downstream the deletion are color coded above the haplotype structure. Haplotype network are shown for genes (D) PROG1, (E) sh4, and (F) sh1. Approximate geographic origins for the causal domestication mutation haplotype and its most closely related ancestral haplotype are shown for genes (G) PROG1, (H) sh4, and (I) sh1. See text for discussion of the hypothesized geographic origins.
Fig 7
Fig 7. Geographical origin of the domestication gene haplotypes.
Haplotypes carrying the domestication mutation are indicated with a star (*). For haplotypes without the casual domestication mutation, only those that are most closely related to the haplotype with the causal mutation are shown. Haplotype numbers and their corresponding relationships are shown in Fig 6.
Fig 8
Fig 8. Panicle threshability scores in O. glaberrima.
(A) Geographical distribution of the panicle threshability scores. (B) Pie chart showing the number of individuals and their panicle threshability scores across the 5 genetic groups designated from this study.
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Grants and funding

This work was supported by grants from the National Science Foundation Plant Genome Research Program (IOS-1546218), the Zegar Family Foundation (A16-0051), and the NYU Abu Dhabi Research Institute (G1205) to M.D.P. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.