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

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 excessmore » 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.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4];  [5];  [6]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [7];  [8]; ORCiD logo [9];  [9]; ORCiD logo [9]; ORCiD logo [10]; ORCiD logo [5]; ORCiD logo [8]; ORCiD logo [8]; ORCiD logo [2] more »; ORCiD logo [11] « less
  1. North Carolina State Univ., Raleigh, NC (United States)
  2. Univ. of Missouri, Columbia, MO (United States)
  3. Michigan State Univ., East Lansing, MI (United States)
  4. Univ. of California, Berkeley, CA (United States)
  5. Univ. of Ottawa, ON (Canada)
  6. Univ. of Saskatchewan, Saskatoon, SK (Canada)
  7. US Dept. of Agriculture (USDA), Columbia, MO (United States)
  8. Univ. of Arizona, Tucson, AZ (United States)
  9. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  10. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  11. North Carolina State Univ., Raleigh, NC (United States); Univ. of Missouri, Columbia, MO (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1813382
Grant/Contract Number:  
AC02-05CH11231; NSF-DBI-1743442; NSF-IOS-2023310; NSF-IOS-1339156
Resource Type:
Accepted Manuscript
Journal Name:
Genome Research
Additional Journal Information:
Journal Volume: 31; Journal Issue: 5; Journal ID: ISSN 1088-9051
Publisher:
Cold Spring Harbor Laboratory Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Hao, Yue, Mabry, Makenzie E., Edger, Patrick P., Freeling, Michael, Zheng, Chunfang, Jin, Lingling, VanBuren, Robert, Colle, Marivi, An, Hong, Abrahams, R. Shawn, Washburn, Jacob D., Qi, Xinshuai, Barry, Kerrie, Daum, Christopher, Shu, Shengqiang, Schmutz, Jeremy, Sankoff, David, Barker, Michael S., Lyons, Eric, Pires, J. Chris, and Conant, Gavin C. The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible. United States: N. p., 2021. Web. doi:10.1101/gr.270033.120.
Hao, Yue, Mabry, Makenzie E., Edger, Patrick P., Freeling, Michael, Zheng, Chunfang, Jin, Lingling, VanBuren, Robert, Colle, Marivi, An, Hong, Abrahams, R. Shawn, Washburn, Jacob D., Qi, Xinshuai, Barry, Kerrie, Daum, Christopher, Shu, Shengqiang, Schmutz, Jeremy, Sankoff, David, Barker, Michael S., Lyons, Eric, Pires, J. Chris, & Conant, Gavin C. The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible. United States. https://doi.org/10.1101/gr.270033.120
Hao, Yue, Mabry, Makenzie E., Edger, Patrick P., Freeling, Michael, Zheng, Chunfang, Jin, Lingling, VanBuren, Robert, Colle, Marivi, An, Hong, Abrahams, R. Shawn, Washburn, Jacob D., Qi, Xinshuai, Barry, Kerrie, Daum, Christopher, Shu, Shengqiang, Schmutz, Jeremy, Sankoff, David, Barker, Michael S., Lyons, Eric, Pires, J. Chris, and Conant, Gavin C. Fri . "The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible". United States. https://doi.org/10.1101/gr.270033.120. https://www.osti.gov/servlets/purl/1813382.
@article{osti_1813382,
title = {The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible},
author = {Hao, Yue and Mabry, Makenzie E. and Edger, Patrick P. and Freeling, Michael and Zheng, Chunfang and Jin, Lingling and VanBuren, Robert and Colle, Marivi and An, Hong and Abrahams, R. Shawn and Washburn, Jacob D. and Qi, Xinshuai and Barry, Kerrie and Daum, Christopher and Shu, Shengqiang and Schmutz, Jeremy and Sankoff, David and Barker, Michael S. and Lyons, Eric and Pires, J. Chris and Conant, Gavin C.},
abstractNote = {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.},
doi = {10.1101/gr.270033.120},
journal = {Genome Research},
number = 5,
volume = 31,
place = {United States},
year = {Fri Apr 16 00:00:00 EDT 2021},
month = {Fri Apr 16 00:00:00 EDT 2021}
}

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