Genes derived from ancient polyploidy have higher genetic diversity and are associated with domestication in Brassica rapa

Abstract

Summary Many crops are polyploid or have a polyploid ancestry. Recent phylogenetic analyses have found that polyploidy often preceded the domestication of crop plants. One explanation for this observation is that increased genetic diversity following polyploidy may have been important during the strong artificial selection that occurs during domestication. In order to test the connection between domestication and polyploidy, we identified and examined candidate genes associated with the domestication of the diverse crop varieties of Brassica rapa. Like all ‘diploid’ flowering plants, B. rapa has a diploidized paleopolyploid genome and experienced many rounds of whole genome duplication (WGD). We analyzed transcriptome data of more than 100 cultivated B. rapa accessions. Using a combination of approaches, we identified > 3000 candidate genes associated with the domestication of four major B. rapa crop varieties. Consistent with our expectation, we found that the candidate genes were significantly enriched with genes derived from the Brassiceae mesohexaploidy. We also observed that paleologs were significantly more diverse than non‐paleologs. Our analyses find evidence for that genetic diversity derived from ancient polyploidy played a key role in the domestication of B. rapa and provide support for its importance in the success of modern agriculture.

The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible

“…We tested for associations between genes' subgenome of origin and their propensity to experience recent selective sweeps. Data on these sweeps was taken from a recent scan in B. rapa by Qi et al (2021). No subgenome had either an excess or a deficit of observed sweeps relative to the other two (Supplemental Fig.…”

“…Association between recent selective sweeps in B. rapa and subgenomes origin B. rapa genes were divided into those in the regions of selective sweeps detected by SweeD (Pavlidis et al 2013) in either turnip, toria, Indian sarson, pak choi, or Chinese cabbage (vegetable types of B. rapa) and those showing no such signatures (Qi et al 2017(Qi et al , 2021. We tested whether particular subgenomes (posterior probability ≥0.95) were unusually likely or unlikely to have experienced a selective sweep using χ 2 test.…”

Diversification, spread, and admixture of octoploid strawberry in the Western Hemisphere

“…With the advent of widespread genome sequencing, the ubiquity of polyploidy across the tree of life, and angiosperms in particular, has been well‐demonstrated (Van de Peer et al, 2017). Polyploidy remains a widely studied evolutionary and ecological phenomena because its hypothesized association with evolution of novel traits (Ohno, 1970; Edger et al, 2015; Van de Peer et al, 2017; Qi et al, 2021) and with species diversification (Schranz et al, 2012; Landis et al, 2018). Despite the ecological and evolutionary importance of polyploidy, polyploid species are underrepresented in existing genomic resources (Marks et al, 2021), largely due to the complexity of assembling polyploid genomes with next‐generation sequencing data (Michael and VanBuren, 2015) and in using reduced representation methods with complex polyploid genomes (Dufresne et al, 2014).…”

Deleterious Mutations Accumulate Faster in Allopolyploid than Diploid Cotton (Gossypium) and Unequally Between Subgenomes

“…Genome duplication (polyploidy) is among the most dramatic mutational processes in nature, causing myriad saltational changes at the cellular and organismal levels (Doyle and Coate 2019;Bomblies 2020;Fernandes Gyorfy et al 2021), and is associated with consequential phenomena ranging from crop domestication (Renny-Byfield and Wendel 2014; Qi et al 2021) to cancer progression (Matsumoto et al 2021). Polyploidy is especially common in the angiosperms, with all extant species having experienced at least one or more polyploidy events during their evolutionary history (Jiao et al 2011), and at least 30% of currently recognized species having a polyploidy event in the recent past (One Thousand Plant Transcriptomes Initiative 2019).…”

“…neofunctionalization, subfunctionalization, and loss (Kuzmin et al 2021)) and genomic (e.g., homoeologous recombination (Mason and Wendel 2020)) levels have been well documented across taxa, including the frequent asymmetry of these responses with respect to co-resident genomes in a polyploid nucleus. Nonetheless, many questions remain regarding the effects of natural selection on polyploid relative to diploid genomes (Baduel et al 2019;Monnahan et al 2019) and the interplay between these novel evolutionary patterns and the long-term trajectories of genome evolution (Qi et al 2021) following polyploidization (e.g. biased fractionation).…”