This analysis was repeated for O. glaberrima and O. barthii separately. Deviation from neutrality of the observed site frequency spectra of the two populations was compared using a two-sample Kolmogorov-Smirnov test. SNPs with a higher Ts:Tv are thus likely to be enriched for true SNPs, while SNPs with a lower Ts:Tv will contain more false positives. The grey bar labelled ‘OB-V and OG’ indicates the smallest monophyletic clade containing all O. glaberrima and its nearest wild relatives. Funding: This study was funded by the National Science Foundation (nsf.gov) Grant No. Filtering criteria with different levels of strictness were applied (S5 Table). Though many of the dishes share similarities, there are variations in nomenclature and differences in the kind of ingredients used. African rice disappeared from the scene because Asian rice was planted when the Arabs took over in 500 to 1000 A.D. MIDDLE EAST Oryza sativa was introduced in the Middle East during the Greek periods (Hellenic and Parthian), and both the Greeks and Romans wrote about it. The relative levels of Tajima’s D suggest that large parts of the O. glaberrima genome exhibit an excess of rare variants as compared to O. barthii. approximately 9000 years ago [1]. Regardless of whether this happened at the onset of domestication or during a secondary wave, the phylogenetic clustering of these haplotypes with different O. barthii accessions provides evidence for a separate genetic origin that may have been caused by introgression or domestication from this otherwise seemingly unrelated wild population. Relative nucleotide diversity was calculated as the ratio of π in O. glaberrima to π in O. barthii, where π defined as: Relative diversity estimates, selection scans and detection of population structure require fewer SNPs; for those analysis, the reduced call set was used. This pattern breaks down when considering phylogenies at the level of individual genes; there we see that some landraces are far removed from the majority of O. glaberrima and cluster with a different O. barthii sub-population instead. In addition, evidence regarding population structure is inconclusive and varies from no observed structure at all [19,21], to clearly differentiated [12,20] and geographically localised [3] sub-populations. No, Is the Subject Area "Single nucleotide polymorphisms" applicable to this article? The three other groups were specific to O. glaberrima and associated with different phenotypic traits, corresponding to the floating, non-floating and upland ecotypes, respectively [20]. [22] merely propose that domestication was centric, but make no claims regarding the rapidity, and Meyer et al. African rice is rarely grown outside sub-Saharan Africa but is of global interest because of its tolerance to abiotic st … No, Is the Subject Area "Haplotypes" applicable to this article? https://doi.org/10.1371/journal.pone.0203508.g004. This reduction in diversity is most likely caused by a combination of selection, favouring a small number of preferred alleles, and demographic history, causing a large drop in effective population size (Ne). The results were deemed sufficiently comparable to proceed with both call sets (S9 Fig). Evolutionary histories were inferred using the NJ algorithm [69] as implemented in MEGA7 [70]. No high-impact substitutions were detected apart from a variant in Sh4 (a shattering gene), which encodes a premature stop codon in almost all domesticated accessions. Values of ω were log-transformed, prior to creating Manhattan plots in R (v3.3.2) using the ‘qqman’ package [52]. Individual genotypes were called using GATK (v3.6.0) HaplotypeCaller on reads with a minimum mapping quality score of 30. Kinship by distance graphs for each population separately and all populations combined can be found in S6 Fig. Allelic differentiation between these populations was measured using Weir and Cockerham’s [41] definition of FST, as implemented in VCFtools (v0.1.14). The selected domestication genes and their proposed functions are listed in S2 Table. Extensive LD is observed in the O. glaberrima genome, with r2 reaching half its maximum value at a distance of 175 kb and approaching baseline at 300 kb [3]. https://doi.org/10.1371/journal.pone.0203508.g001. Center for Genomics and Systems Biology, New York University Abu Dhabi, Saadiyat Island, Abu Dhabi, United Arab Emirates, Roles Rice accompanied African slaves across the Middle Passage throughout the New World to Brazil, the Caribbean, and the southern United States. To confirm the clustering of O. glaberrima within O. barthii, a whole genome phylogenetic tree was constructed based on 3,923,601 genome-wide SNPs. Answer! A joint ADMIXTURE analysis was performed to infer which ancestor fractions are shared between the species and which are unique. Although the exact history of rice in Asia is still disputed, it is clear that Asian rice (Oryza sativa L.) was domesticated from a single wild species (Oryza rufipogon Griff.) D. Isolation by distance among the inland populations (OG-IV and OG-V). Because the African rice genome is poorly annotated, their putative location in the O. glaberrima genome was determined using the O. sativa reference genome as a guide. Whereas N denotes the number of accessions included in each analysis, the number of pairwise comparison equals N! here. Interestingly, all the accessions that originate from the proposed primary domestication centre of African rice, around the Inner Niger Delta (Fig 1B), belong to a single genetic cluster (OG-V). The population structure of African rice further sheds light on the geography of its domestication. Untrimmed reads were mapped to the reference genome using the BWA-MEM algorithm [35] of the Burrows-Wheeler Aligner (v0.7.13). Despite these limitations, the marked population structure observed in O. glaberrima points to geographic differentiation during or following domestication. The excess of rare variants in O. glaberrima is confirmed by the Minor Allele Frequency (MAF) spectrum (S2 Fig), where O. glaberrima has a larger spike in low frequency alleles (MAF < 0.01) than the majority of O. barthii alleles, which are of intermediate frequency (MAF 0.01–0.05). So! In addition, focus should be given to more even sampling across the geographic range of both species, especially in the eastern range for O. glaberrima and in the western range for O. barthii, where collections of these species are presently scarce. While SweeD is capable of taking into account the polarisation of alleles in the so-called ‘unfolded’ SFS, this has the disadvantage that limiting the analyses to only unfolded SNPs causes a significant loss of data. Here aibi is the genotype at position i in X, and cidi is the genotype at position i in Y. Cross-validation error estimates of all three analyses can be found in S5 Fig. Whether this stems from methodological issues or from the population structure observed in O. glaberrima can only be demonstrated with improved knowledge of the demographic history of O. glaberrima and additional modelling. Biosystematics Group, Wageningen University and Research, Wageningen, The Netherlands, Roles endobj This article begins with information about the past and present status of African rice and then moves to a detailed example of when, how, and why it was cultivated by the Jola, a population of ancient rice growing peoples living in the swampy coastal areas of Casamance, in southern Senegal. Genetic IBD was discernible among the coastal populations with a correlation coefficient (r) of -0.35 (Fig 4). Putative effects of segregating SNPs were predicted using SnpEff (v4.0). Both the negative values of Tajima’s D and the skewed MAF distribution in favour of rare alleles support the notion that O. glaberrima underwent population expansion following a severe bottleneck. This recurrent pattern stands in stark contrast with the genome-wide phylogeny, where the OB-B population is genetically most distant from O. glaberrima (Fig 5). Based on the results by Meyer et al. A. Each dot symbolises a unique pair of individuals within in each group. [3], who separated African rice into groups based on a 11°N and the 6°W cline. Click through the PLOS taxonomy to find articles in your field. To determine the degree of genetic differentiation between the geographic regions, the fixation index (FST) was calculated between individuals separated by the 11°N and the 6°W cline, respectively. endobj A. NJ tree with all O. barthii (OB) and O. glaberrima (OG) accessions. A distantly related outgroup circumvents this problem but is more difficult to align, and hence will cause larger loss of data. Oryza glaberrima, commonly known as African rice, is one of the two domesticated rice species. Globalisation places these local cultural traditions and the neglected species associated with them under threat [6]. But perhaps the most compelling argument that can be made against the hard sweep model in O. glaberrima, is the population subdivision. Thus, while many questions concerning the domestication and migration of African rice are still outstanding, the complete genome sequences of more than a hundred O. glaberrima accessions—and an almost equal number of O. barthii accessions—provide a wealth of genetic data that can be used to reconstruct the evolutionary history of African rice, and to compare the genetic diversity of O. glaberrima in its different localities. https://doi.org/10.1371/journal.pone.0203508.s001, https://doi.org/10.1371/journal.pone.0203508.s002, https://doi.org/10.1371/journal.pone.0203508.s003, https://doi.org/10.1371/journal.pone.0203508.s004, https://doi.org/10.1371/journal.pone.0203508.s005, https://doi.org/10.1371/journal.pone.0203508.s006, https://doi.org/10.1371/journal.pone.0203508.s007, https://doi.org/10.1371/journal.pone.0203508.s008, https://doi.org/10.1371/journal.pone.0203508.s009, https://doi.org/10.1371/journal.pone.0203508.s010, https://doi.org/10.1371/journal.pone.0203508.s011, https://doi.org/10.1371/journal.pone.0203508.s012, https://doi.org/10.1371/journal.pone.0203508.s013, https://doi.org/10.1371/journal.pone.0203508.s014, https://doi.org/10.1371/journal.pone.0203508.s015, https://doi.org/10.1371/journal.pone.0203508.s016, https://doi.org/10.1371/journal.pone.0203508.s017, https://doi.org/10.1371/journal.pone.0203508.s018, https://doi.org/10.1371/journal.pone.0203508.s019. In comparative analyses of a number of these CLR methods using simulated data, SweeD and OmegaPlus were shown to outperform other tests [50]. A study of genetic diversity based on 235 single nucleotide polymorphisms (SNPs) also found two distinct populations in 266 O. glaberrima accessions without any correlation to geography—in contrast to their wild relative, which clustered into three geographically distinct sub-populations [12]. The ω test statistic is calculated as: and is therefore markedly higher. The diversity measures reported in this study are consistent with previous reports [3,22] and provide strong evidence for a large reduction in diversity in the genome of O. glaberrima as a result of domestication. 2007-09-12T10:24:36ZMicrosoft® Office Word 20072013-04-16T17:11:49+01:00 At least twice, say scholars, a manipulation of japonica rice was required: in the Indian subcontinent about 2500 BC, and in West Africa between 1500 and 800 BCE. (S7 Table). https://doi.org/10.1371/journal.pone.0203508.g006. Evolutionary distances were calculated using the p-distance method of Nei & Kumar [71]. These sequences are linked to under BioProjects PRJNA13765, PRJNA30379, PRJNA315063 and PRJNA514989. This is compatible with the general trend in π ratio (πw/ πc), which is usually well above one (S2 Fig) and takes on particularly high values when Tajima’s D is extremely negative. The fourth objective was met by mapping a principal components analysis onto known geographic coordinates and measuring isolation by distance. A closer examination of the genetic diversity and signatures of selection of the hypothetical ancestor population in comparison to other O. barthii and O. glaberrima accessions might elucidate whether they are more similar to the domesticated or to the wild species. The first principal component is correlated significantly with longitude and the second principal component is correlated significantly with latitude. Output was converted to FASTA format with a custom perl script. The divergence between two genomes X and Y was calculated as: Yes https://doi.org/10.1371/journal.pone.0203508.t001. & Roehr. Filter thresholds were determined based on their effect on the Transition:Transversion ratio (Ts:Tv). https://doi.org/10.1371/journal.pone.0203508.t004. Several studies have tried to illuminate the question of how and where African rice originated, either implicitly or explicitly addressing the domestication hypotheses described above. This event resulted in a species that is now recognised as Oryza glaberrima Steud. The geographic component of population structure can prevent instances of position selection from sweeping through the entire population in multiple ways. Tajima’s D was significantly different between the two species at p < 1.0E-05, being predominantly negative in O. glaberrima (-0.6761) and positive in O. barthii (0.5172). Although there are some indications of positive selection in terms of an excess of high frequency derived alleles, conclusive evidence of hard selective sweeps—especially in relation to known domestication traits—has been elusive. https://doi.org/10.1371/journal.pone.0203508.t003. [20] found five cryptic sub-populations based on a study of 93 microsatellite markers in 198 O. glaberrima and 9 O. sativa accessions. The top 20 principal components were calculated for both species together and for both species separately using PLINK (v1.9). In addition, O. glaberrima and O. barthii diverged so recently that hybridisation is still considered possible—if difficult—and that admixture between O. barthii and O. glaberrima even now should not be excluded. To verify whether these candidate regions show other characteristic signatures of selection, the ω-statistic was plotted against overlapping 25 kb windows of π and Tajima’s D, respectively (S4 Fig). Since the non-shattering phenotype is a crucial trait in the domestication syndrome, the ancestral state of this substitution in a limited number of OG-II accessions presupposes that another variant—either in the same gene or in a different gene—might be causing the same phenotype. This study used publicly available whole genome data of 111 O. glaberrima and 94 O. barthii accessions. We thus observe that, even though the total number of polymorphic sites in larger in OG-I through OG-III, the average number of pairwise differences between these individuals is lower. Genomic features containing putative moderate to high impact mutations within close proximity (< 25 kb) of candidate regions were extracted for closer inspection using a custom R script. In addition, this test does not consider alternative forms of selection, such as balancing selection or diversifying selection. In these genes, a subset of O. glaberrima from a single subpopulation cluster together in smaller clades that are far removed from the larger O. glaberrima clade. Yes The genus Oryza is among the most ancient grasses and was able to spread to every continent before they drifted too far apart. Although some candidate genes that were scanned in the CLR test are not necessarily expected to be under universal selection in African rice because of their biological function (such as COLD1), other genes that we expected to be among the outliers (such as Sh4) also lacked a clear signal, casting doubt on the assumptions of the employed method. application/pdfOverseas Development InstituteThe history of rice in West Africa - Accessions are labelled by species and coloured according to their genetic cluster (K = 8). As a matter of fact, Jollof rice probably traveled to America too, as jambalaya and especially Lowcountry red rice share a lot of similarities with Jollof rice. Archaeologists have found ceramic impressions of rice grains dating from 1800 bc to 800 bc in Ganjigana located in north-east Nigera. This has recently been confirmed by functional characterisation of another gene, called Sh3, that is on its own responsible for a non-shattering phenotype in African rice [26]. PLOS ONE promises fair, rigorous peer review, B. We did not filter for heterozygous sites, because both species are primarily inbreeding and therefore exhibit low levels of heterozygosity. In contrast, OG-IV is restricted to the inland areas and is located primarily south and east of OG-V. Phylogenetic analysis shows that the exact same OG-II accessions form a separate haplotype in this gene as in Sd1 (Table 3). Although this is well outside the zone of cultivation today, African rice was probably common in the Sahara in wetter periods (Chevalier, 1932:86). Formal analysis, The other proposes a centric (geographically localised) domestication along the Niger River, followed by two secondary diversification events: one along the coast of what are now the countries of Senegal and Gambia, and one in the Guinea Highlands [2]. Variant discovery was performed following the Genome Analysis Tool Kit (GATK) Best Practices [34]. 2 0 obj The present distribution of O. glaberrima cultivation in West Africa is shaded in light green, based on Vaughan [18]. This excess is also caused by higher frequency classes in O. glaberrima (21% of total SNPs > 0.99) than in O. barthii (18% of total SNPs > 0.95). Eight of the twenty genes clearly deviate from the genome-wide phylogenetic signal (S3 Table). Pairwise genomic distances between all accessions were calculated using a custom perl script, implementing the method described in S3.2 of [59].