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

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

doi:10.1186/s13059-019-1729-9

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

Journal Article · Fri Jun 21 00:00:00 EDT 2019 · Genome Biology (Online)

DOI:https://doi.org/10.1186/s13059-019-1729-9· OSTI ID:1580886

^[1]; Mojica, Julius P. ^[2]; Perera, Nadeesha ^[2]; Lee, Cheng -Ruei ^[3]; Lovell, John T. ^[4]; Sharma, Aditi ^[5]; Adam, Catherine ^[5]; Lipzen, Anna ^[5]; Barry, Kerrie ^[5]; Rokhsar, Daniel S. ^[5]; Schmutz, Jeremy ^[6]; Mitchell-Olds, Thomas ^[2]

Chinese Academy of Sciences, Guangzhou (China); Duke Univ., Durham, NC (United States)
Duke Univ., Durham, NC (United States)
National Taiwan Univ., Taipei (Taiwan)
HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

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 (d_XY), and lower relative divergence (F_ST) 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 F_ST and d_XY among the groups, termed F_ST-islands. Population genetic signatures indicate that F_ST-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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1580886

Journal Information:: Genome Biology (Online), Vol. 20, Issue 1; ISSN 1474-760X

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 22 works

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Additional file 1: of Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta Wang, Baosheng; Mojica, Julius; Perera, Nadeesha https://doi.org/10.6084/m9.figshare.8310347 The current record is supplemented by this text	text	January 2019
Additional file 1: of Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta Wang, Baosheng; Mojica, Julius; Perera, Nadeesha https://doi.org/10.6084/m9.figshare.8310347.v1 The current record is supplemented by this text	text	January 2019
Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta Wang, Baosheng; Mojica, Julius; Perera, Nadeesha https://doi.org/10.6084/m9.figshare.c.4551557 The current record is supplemented by this collection	collection	January 2019
Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta Wang, Baosheng; Mojica, Julius; Perera, Nadeesha https://doi.org/10.6084/m9.figshare.c.4551557.v1 The current record is supplemented by this collection	collection	January 2019