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Title: Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta

Abstract

Genomic variation is widespread, and both neutral and selective processes can generate similar patterns in the genome. These processes are not mutually exclusive, so it is difficult to infer the evolutionary mechanisms that govern population and species divergence. Boechera stricta is a perennial relative of Arabidopsis thaliana native to largely undisturbed habitats with two geographic and ecologically divergent subspecies. Here, we delineate the evolutionary processes driving the genetic diversity and population differentiation in this species. Using whole-genome re-sequencing data from 517 B. stricta accessions, we identify four genetic groups that diverged around 30-180 thousand years ago, with long-term small effective population sizes and recent population expansion after the Last Glacial Maximum. We find three genomic regions with elevated nucleotide diversity, totaling about 10% of the genome. These three regions of elevated nucleotide diversity show excess of intermediate-frequency alleles, higher absolute divergence (dXY), and lower relative divergence (FST) than genomic background, and significant enrichment in immune-related genes, reflecting long-term balancing selection. Scattered across the genome, we also find regions with both high FST and dXY among the groups, termed FST-islands. Population genetic signatures indicate that FST-islands with elevated divergence, which have experienced directional selection, are derived from divergent sorting of ancientmore » polymorphisms. Our results suggest that long-term balancing selection on disease resistance genes may have maintained ancestral haplotypes across different geographical lineages, and unequal sorting of balanced polymorphisms may have generated genomic regions with elevated divergence. This study highlights the importance of ancestral balanced polymorphisms as crucial components of genome-wide variation.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3];  [4];  [5];  [5];  [5];  [5];  [5];  [6];  [2]
  1. Chinese Academy of Sciences, Guangzhou (China); Duke Univ., Durham, NC (United States)
  2. Duke Univ., Durham, NC (United States)
  3. National Taiwan Univ., Taipei (Taiwan)
  4. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1580886
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Genome Biology (Online)
Additional Journal Information:
Journal Name: Genome Biology (Online); Journal Volume: 20; Journal Issue: 1; Journal ID: ISSN 1474-760X
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Genomic diversity; Ancestral polymorphism; Balancing selection; Speciation

Citation Formats

Wang, Baosheng, Mojica, Julius P., Perera, Nadeesha, Lee, Cheng -Ruei, Lovell, John T., Sharma, Aditi, Adam, Catherine, Lipzen, Anna, Barry, Kerrie, Rokhsar, Daniel S., Schmutz, Jeremy, and Mitchell-Olds, Thomas. Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta. United States: N. p., 2019. Web. doi:10.1186/s13059-019-1729-9.
Wang, Baosheng, Mojica, Julius P., Perera, Nadeesha, Lee, Cheng -Ruei, Lovell, John T., Sharma, Aditi, Adam, Catherine, Lipzen, Anna, Barry, Kerrie, Rokhsar, Daniel S., Schmutz, Jeremy, & Mitchell-Olds, Thomas. Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta. United States. https://doi.org/10.1186/s13059-019-1729-9
Wang, Baosheng, Mojica, Julius P., Perera, Nadeesha, Lee, Cheng -Ruei, Lovell, John T., Sharma, Aditi, Adam, Catherine, Lipzen, Anna, Barry, Kerrie, Rokhsar, Daniel S., Schmutz, Jeremy, and Mitchell-Olds, Thomas. Fri . "Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta". United States. https://doi.org/10.1186/s13059-019-1729-9. https://www.osti.gov/servlets/purl/1580886.
@article{osti_1580886,
title = {Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta},
author = {Wang, Baosheng and Mojica, Julius P. and Perera, Nadeesha and Lee, Cheng -Ruei and Lovell, John T. and Sharma, Aditi and Adam, Catherine and Lipzen, Anna and Barry, Kerrie and Rokhsar, Daniel S. and Schmutz, Jeremy and Mitchell-Olds, Thomas},
abstractNote = {Genomic variation is widespread, and both neutral and selective processes can generate similar patterns in the genome. These processes are not mutually exclusive, so it is difficult to infer the evolutionary mechanisms that govern population and species divergence. Boechera stricta is a perennial relative of Arabidopsis thaliana native to largely undisturbed habitats with two geographic and ecologically divergent subspecies. Here, we delineate the evolutionary processes driving the genetic diversity and population differentiation in this species. Using whole-genome re-sequencing data from 517 B. stricta accessions, we identify four genetic groups that diverged around 30-180 thousand years ago, with long-term small effective population sizes and recent population expansion after the Last Glacial Maximum. We find three genomic regions with elevated nucleotide diversity, totaling about 10% of the genome. These three regions of elevated nucleotide diversity show excess of intermediate-frequency alleles, higher absolute divergence (dXY), and lower relative divergence (FST) than genomic background, and significant enrichment in immune-related genes, reflecting long-term balancing selection. Scattered across the genome, we also find regions with both high FST and dXY among the groups, termed FST-islands. Population genetic signatures indicate that FST-islands with elevated divergence, which have experienced directional selection, are derived from divergent sorting of ancient polymorphisms. Our results suggest that long-term balancing selection on disease resistance genes may have maintained ancestral haplotypes across different geographical lineages, and unequal sorting of balanced polymorphisms may have generated genomic regions with elevated divergence. This study highlights the importance of ancestral balanced polymorphisms as crucial components of genome-wide variation.},
doi = {10.1186/s13059-019-1729-9},
journal = {Genome Biology (Online)},
number = 1,
volume = 20,
place = {United States},
year = {Fri Jun 21 00:00:00 EDT 2019},
month = {Fri Jun 21 00:00:00 EDT 2019}
}

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Works referencing / citing this record:

Correction to: Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta
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