The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible
- Yue Hao1,
- Makenzie E. Mabry2,
- Patrick P. Edger3,4,
- Michael Freeling5,
- Chunfang Zheng6,
- Lingling Jin7,
- Robert VanBuren3,8,
- Marivi Colle3,
- Hong An2,
- R. Shawn Abrahams2,
- Jacob D. Washburn9,
- Xinshuai Qi10,
- Kerrie Barry11,
- Christopher Daum11,
- Shengqiang Shu11,
- Jeremy Schmutz11,12,
- David Sankoff6,
- Michael S. Barker10,
- Eric Lyons13,14,
- J. Chris Pires2,15 and
- Gavin C. Conant1,16,17,18
- 1Bioinformatics Research Center, North Carolina State University, Raleigh, North Carolina 27695, USA;
- 2Division of Biological Sciences, University of Missouri–Columbia, Columbia, Missouri 65211, USA;
- 3Department of Horticulture, Michigan State University, East Lansing, Michigan 48824, USA;
- 4Genetics and Genome Sciences, Michigan State University, East Lansing, Michigan 48824, USA;
- 5Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA;
- 6Department of Mathematics and Statistics, University of Ottawa, Ottawa, Ontario K1N 6N5, Canada;
- 7Department of Computer Science, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5C9, Canada;
- 8Plant Resilience Institute, Michigan State University, East Lansing, Michigan 48824, USA;
- 9Plant Genetics Research Unit, USDA-ARS, Columbia, Missouri 65211, USA;
- 10Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA;
- 11Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA;
- 12HudsonAlpha Institute for Biotechnology, Huntsville, Alabama 35806, USA;
- 13School of Plant Sciences, University of Arizona, Tucson, Arizona 85721, USA;
- 14BIO5 Institute, University of Arizona, Tucson, Arizona 85721, USA;
- 15Informatics Institute, University of Missouri–Columbia, Columbia, Missouri 65211, USA;
- 16Program in Genetics, North Carolina State University, Raleigh, North Carolina 27695, USA;
- 17Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina 27695, USA;
- 18Division of Animal Sciences, University of Missouri–Columbia, Columbia, Missouri 65211, USA
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 which subgenome origin drives homoeolog loss propensities but where genes from different subgenomes function together without difficulty.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.270033.120.
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Freely available online through the Genome Research Open Access option.
- Received August 10, 2020.
- Accepted March 5, 2021.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
