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

Authors: HAO, YUE - North Carolina State University; MABRY, MAKENZIE - University Of Missouri; EDGER, PATRICK - Michigan State University; FREELING, MICHAEL - University Of California; ZHENG, CHUNFANG - University Of Ottawa; JIN, LINGLING - Thompson Rivers University; VANBUREN, ROBERT - Michigan State University; COLLE, MARIVI - Michigan State University; AN, HONG - University Of Missouri; ABRAHAMS, RICHARD - University Of Missouri; Washburn, Jacob; QI, XINSHUAI - University Of Arizona; BARRY, KERRIE - Berkeley National Laboratory; DAUM, CHRISTOPHER - Berkeley National Laboratory; SHU, SHENGQIANG - Berkeley National Laboratory; SCHMUTZ, JEREMY - Berkeley National Laboratory; SANKOFF, DAVID - University Of Ottawa; BARKER, MICHAEL - University Of Arizona; LYONS, ERIC - University Of Arizona; PIRES, CHRIS - University Of Missouri; CONANT, GAVIN - North Carolina State University

Submitted to: Genome Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/5/2021
Publication Date: 4/16/2021
Citation: Hao, Y., Mabry, M.E., Edger, P.P., Freeling, M., Zheng, C., Jin, L., VanBuren, R., Colle, M., An, H., Abrahams, R.S., Washburn, J.D., Qi, X., Barry, K., Daum, C., Shu, S., Schmutz, J., Sankoff, D., Barker, M.S., Lyons, E., Pires, C.J., Conant, G.C. 2021. The contributions from the progenitor genomes of the mesopolyploid brassiceae are evolutionarily distinct but functionally compatible. Genome Research. 31(5):799-810. https://doi.org/10.1101/gr.270033.120.
DOI: https://doi.org/10.1101/gr.270033.120

Interpretive Summary: Many agricultural crops contain ancient whole genome duplications. These duplications have been linked to important adaptations in both wild and domesticated species. Understanding how and when these events occurred can provide insights into future crop improvement, domestication of new crops from wild species, and moving important traits from crop wild relatives into modern varieties. The tribe Brassiceae (in the mustard family) is a perfect place to study these processes and apply them to crop improvement. The formation of a whole genome triplication event in the Brassiceae has been a subject of study since its discover. Here we report the sequencing of an additional Brassiceae genome and analyses that confirm the previous hypothesis that the Brassiceae whole genome triplication event occurred as a two-step process. Based on these findings, a "mix and match" model for understanding the formation and evolution polyploid species is proposed.

Technical Abstract: The members of the tribe Brassiceae share a whole-genome triplication (WGT), and one proposed model for its formation is a two-step pair of hybridizations producing hexaploid descendants. However, evidence for this model is incomplete, and 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. Using this new genome and three others that share the hexaploidy, we traced the history of gene loss after the WGT using the Polyploidy Orthology Inference Tool (POInT). We confirm the two-step formation model and infer that there was a significant temporal gap between those two allopolyploidizations, with about a third of the gene losses from the first two subgenomes occurring before the arrival of the third. We also, for the 90,000 individual genes in our study, make parental subgenome assignments, inferring, with measured uncertainty, from which of the progenitor genomes of the allohexaploidy each gene derives. We further show that each subgenome has a statistically distinguishable rate of homoeolog losses. 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, in whichsubgenome origin drives homoeolog loss propensities but where genes from different subgenomes function together without difficulty.