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

Abstract

The members of the tribe Brassiceae share an ancient whole genome triplication (WGT), and plants in this tribe display extraordinarily high within-species morphological diversity. One proposed model for the formation of these hexaploid Brassiceae is that they result from a “two-step” pair of hybridizations. However, direct evidence supporting this model of formation has been lacking; meanwhile, the evolutionary and functional constraints that drove evolution after the hexaploidy are even less understood. Here we report a new genome sequence of Crambe hispanica, a species sister to most sequenced Brassiceae. After adding this new genome to three others that are also descended from the ancient hexaploidy, we traced the history of gene loss after the WGT using a phylogenomic pipeline called POInT (the Polyploidy Orthology Inference Tool). This approach allowed us to confirm the two-step model of hexaploidy formation and to assign statistical confidence to our parental “subgenome” assignments for >90,000 individual genes. We show that each subgenome has a statistically distinguishable rate of homeolog losses. Moreover, our modeling allowed us to infer that there was a significant temporal gap between the two allopolyploidizations, with about one third of the total shared gene losses between the four analyzed Brassiceae species in the first two subgenomes prior to the arrival of the third subgenome. There is little indication of functional distinction between the three subgenomes: the individual subgenomes show no patterns of functional enrichment, no excess of shared protein-protein or metabolic interactions between their members, and no biases in their likelihood of having experienced a recent selective sweep. We propose a “mix and match” model of allopolyploidy, where subgenome origin drives homeolog loss propensities but where genes from different subgenomes function together without difficulty.

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

“…(b) Phylogeny of species’s genomes used for the POI n T multi‐genome analysis to identify paleologs in B. rapa from Hao et al . (2020). A total of 13 499 paleologs and 27 527 non‐paleologs were identified in B. rapa .…”

“…We also used results from a recent multi‐genome comparative analysis (Hao et al ., 2020) to infer paleologs in B. rapa . A recent POI n T analysis of the genomes for four Brassiceae species ( B. oleracea , B. rapa , C. hispanica and S. alba ) uncovered evidence for 14 050 regions (‘pillars’ in POI n T terminology) of triple conserved synteny from the Brassiceae mesohexaploidy across the four genomes.…”

“…We also developed a second set of paleologs and nonpalelogs from a recent multigenome comparative analysis with POI n T, the Polyploidy Orthology Inference Tool (Hao et al ., 2020). The POI n T analysis modeled the history of genome evolution following the Brassiceae mesohexaploidy by comparing the genomes of Arabidopsis thaliana , Brassica oleracea , B. rapa , Crambe hispanica and Sinapis alba .…”

“…POINT uses a probabilistic approach to assess if a gene belongs to a paleolog pillar. We filtered for genes in the B. rapa genome that had a > 95% probability of assignment to one of these mesohexaploid pillars from the Hao et al (2020) analysis. These data were used to develop a list of B. rapa paleologs that were retained in single, double or triple copy from the ancient hexaploidy.…”

“…Genes that were not present in any of the three paleologs lists were considered to be non-paleologs. (b) Phylogeny of species's genomes used for the POINT multi-genome analysis to identify paleologs in B. rapa from Hao et al (2020). A total of 13 499 paleologs and 27 527 non-paleologs were identified in B. rapa.…”