Multiple origins, one evolutionary trajectory: gradual evolution characterizes distinct lineages of allotetraploid Brachypodium

Scarlett, Virginia T.; Lovell, John T.; Shao, Mingqin; Phillips, Jeremy; Shu, Shengqiang; Lusinska, Joanna; Goodstein, David M.; Jenkins, Jerry; Grimwood, Jane; Barry, Kerrie; Chalhoub, Boulos; Schmutz, Jeremy; Hasterok, Robert; Catalán, Pilar; Vogel, John P.

doi:10.1093/genetics/iyac146

Multiple origins, one evolutionary trajectory: gradual evolution characterizes distinct lineages of allotetraploid Brachypodium

Journal Article · Tue Oct 11 00:00:00 EDT 2022 · Genetics (Online)

DOI:https://doi.org/10.1093/genetics/iyac146· OSTI ID:2422823

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USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
University of Silesia, Katowice (Poland)
Agroscope (Switzerland)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
University of Zaragoza (Spain)

The “genomic shock” hypothesis posits that unusual challenges to genome integrity such as whole genome duplication may induce chaotic genome restructuring. Decades of research on polyploid genomes have revealed that this is often, but not always the case. While some polyploids show major chromosomal rearrangements and derepression of transposable elements in the immediate aftermath of whole genome duplication, others do not. Nonetheless, all polyploids show gradual diploidization over evolutionary time. To evaluate these hypotheses, we produced a chromosome-scale reference genome for the natural allotetraploid grass Brachypodium hybridum, accession “Bhyb26.” We compared 2 independently derived accessions of B. hybridum and their deeply diverged diploid progenitor species Brachypodium stacei and Brachypodium distachyon. The 2 B. hybridum lineages provide a natural timecourse in genome evolution because one formed 1.4 million years ago, and the other formed 140 thousand years ago. The genome of the older lineage reveals signs of gradual post-whole genome duplication genome evolution including minor gene loss and genome rearrangement that are missing from the younger lineage. In neither B. hybridum lineage do we find signs of homeologous recombination or pronounced transposable element activation, though we find evidence supporting steady post-whole genome duplication transposable element activity in the older lineage. Gene loss in the older lineage was slightly biased toward 1 subgenome, but genome dominance was not observed at the transcriptomic level. We propose that relaxed selection, rather than an abrupt genomic shock, drives evolutionary novelty in B. hybridum, and that the progenitor species’ similarity in transposable element load may account for the subtlety of the observed genome dominance.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2422823

Journal Information:: Genetics (Online), Journal Name: Genetics (Online) Journal Issue: 2 Vol. 223; ISSN 1943-2631

Publisher:: Oxford University Press; Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

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MITE Tracker: an accurate approach to identify miniature inverted-repeat transposable elements in large genomes Crescente, Juan Manuel; Zavallo, Diego; Helguera, Marcelo Figshare https://doi.org/10.6084/m9.figshare.c.4253741	collection	January 2018
Dynamic and reversible DNA methylation changes induced by genome separation and merger of polyploid wheat Yuan, Jingya; Jiao, Wu; Liu, Yanfeng figshare https://doi.org/10.6084/m9.figshare.c.5214773.v1	collection	January 2020

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59 BASIC BIOLOGICAL SCIENCES
Brachypodium
fractionation
genome dominance
genomics
plant genetics and genomics
polyploidy
structural variation
transposable element dynamics

Multiple origins, one evolutionary trajectory: gradual evolution characterizes distinct lineages of allotetraploid Brachypodium

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