Transcriptome population genomics reveals severe bottleneck and domestication cost in the African rice (Oryza glaberrima)

Abstract

The African cultivated rice (Oryza glaberrima) was domesticated in West Africa 3000 years ago. Although less cultivated than the Asian rice (O. sativa), O. glaberrima landraces often display interesting adaptation to rustic environment (e.g. drought). Here, using RNA-seq technology, we were able to compare more than 12,000 transcripts between 9 O. glaberrima, 10 wild O. barthii and one O. meridionalis individuals. With a synonymous nucleotide diversity πs = 0.0006 per site, O. glaberrima appears as the least genetically diverse crop grass ever documented. Using approximate Bayesian computation, we estimated that O. glaberrima experienced a severe bottleneck during domestication. This demographic scenario almost fully accounts for the pattern of genetic diversity across O. glaberrima genome as we detected very few outliers regions where positive selection may have further impacted genetic diversity. Moreover, the large excess of derived nonsynonymous substitution that we detected suggests that the O. glaberrima population suffered from the 'cost of domestication'. In addition, we used this genome-scale data set to demonstrate that (i) O. barthii genetic diversity is positively correlated with recombination rate and negatively with gene density, (ii) expression level is negatively correlated with evolutionary constraint, and (iii) one region on chromosome 5 (position 4-6 Mb) exhibits a clear signature of introgression with a yet unidentified Oryza species. This work represents the first genome-wide survey of the African rice genetic diversity and paves the way for further comparison between the African and the Asian rice, notably regarding the genetics underlying domestication traits.

de novo assemblies of three Oryza glaberrima accessions provide first insights about pan-genome of African rices

“…We then aimed to find large divergence within those sequences, and decided to check the (micro-)collinearity status of our assemblies, and found that around 25% of the genome present enough variation to lead to collinearity breakdown. As shown on Asian rice (Sakai et al 2014; Schatz et al 2014; Zhang et al 2016), we identified thus large scale variations and thus a larger pan-genomic space than what could have been expected based only on SNP data (Nabholz et al 2014; Orjuela et al 2014). Interestingly, we found around 0.6% of our scaffolds to be absent in one assembly regarding another one.…”

Prehistoric genomes reveal the genetic foundation and cost of horse domestication

“…Previous scans of domesticated genomes have revealed an accumulation of deleterious mutations in rice (62,63), tomatoes (64), and dogs (4). This phenomenon has been termed the "cost of domestication" and is proposed to be driven by the repetitive bottlenecks associated with domestication, which reduce the efficiency of purifying selection (4).…”

Next‐generation metrics for monitoring genetic erosion within populations of conservation concern

“…When considering genetic monitoring and management, these approaches provide the opportunity to assess, first, the gene variant(s) behind the traits identified and the evolution of the frequency of those variants. This issue is particularly important in domestic populations, where artificial selection has resulted in accumulation of deleterious mutations (Charlier et al., ; Nabholz et al., ; Summers, Diesel, Asher, McGreevy, & Collins, ). Management of deleterious mutations may be integrated within selection and conservation schemes (see Box ).…”