Gene disruption by structural mutations drives selection in US rice breeding over the last century.

The genetic basis of general plant vigor is of major interest to food producers, yet the trait is recalcitrant to genetic mapping because of the number of loci involved, their small effects, and linkage. Observations of heterosis in many crops suggests that recessive, malfunctioning versions of gene...

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Main Authors: Justin N Vaughn, Walid Korani, Joshua C Stein, Jeremy D Edwards, Daniel G Peterson, Sheron A Simpson, Ramey C Youngblood, Jane Grimwood, Kapeel Chougule, Doreen H Ware, Anna M McClung, Brian E Scheffler
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-03-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009389&type=printable
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author Justin N Vaughn
Walid Korani
Joshua C Stein
Jeremy D Edwards
Daniel G Peterson
Sheron A Simpson
Ramey C Youngblood
Jane Grimwood
Kapeel Chougule
Doreen H Ware
Anna M McClung
Brian E Scheffler
author_facet Justin N Vaughn
Walid Korani
Joshua C Stein
Jeremy D Edwards
Daniel G Peterson
Sheron A Simpson
Ramey C Youngblood
Jane Grimwood
Kapeel Chougule
Doreen H Ware
Anna M McClung
Brian E Scheffler
author_sort Justin N Vaughn
collection DOAJ
description The genetic basis of general plant vigor is of major interest to food producers, yet the trait is recalcitrant to genetic mapping because of the number of loci involved, their small effects, and linkage. Observations of heterosis in many crops suggests that recessive, malfunctioning versions of genes are a major cause of poor performance, yet we have little information on the mutational spectrum underlying these disruptions. To address this question, we generated a long-read assembly of a tropical japonica rice (Oryza sativa) variety, Carolina Gold, which allowed us to identify structural mutations (>50 bp) and orient them with respect to their ancestral state using the outgroup, Oryza glaberrima. Supporting prior work, we find substantial genome expansion in the sativa branch. While transposable elements (TEs) account for the largest share of size variation, the majority of events are not directly TE-mediated. Tandem duplications are the most common source of insertions and are highly enriched among 50-200bp mutations. To explore the relative impact of various mutational classes on crop fitness, we then track these structural events over the last century of US rice improvement using 101 resequenced varieties. Within this material, a pattern of temporary hybridization between medium and long-grain varieties was followed by recent divergence. During this long-term selection, structural mutations that impact gene exons have been removed at a greater rate than intronic indels and single-nucleotide mutations. These results support the use of ab initio estimates of mutational burden, based on structural data, as an orthogonal predictor in genomic selection.
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spelling doaj-art-a0ec0b5a32034b8ba97a9803c685d0a32025-08-20T02:55:20ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-03-01173e100938910.1371/journal.pgen.1009389Gene disruption by structural mutations drives selection in US rice breeding over the last century.Justin N VaughnWalid KoraniJoshua C SteinJeremy D EdwardsDaniel G PetersonSheron A SimpsonRamey C YoungbloodJane GrimwoodKapeel ChouguleDoreen H WareAnna M McClungBrian E SchefflerThe genetic basis of general plant vigor is of major interest to food producers, yet the trait is recalcitrant to genetic mapping because of the number of loci involved, their small effects, and linkage. Observations of heterosis in many crops suggests that recessive, malfunctioning versions of genes are a major cause of poor performance, yet we have little information on the mutational spectrum underlying these disruptions. To address this question, we generated a long-read assembly of a tropical japonica rice (Oryza sativa) variety, Carolina Gold, which allowed us to identify structural mutations (>50 bp) and orient them with respect to their ancestral state using the outgroup, Oryza glaberrima. Supporting prior work, we find substantial genome expansion in the sativa branch. While transposable elements (TEs) account for the largest share of size variation, the majority of events are not directly TE-mediated. Tandem duplications are the most common source of insertions and are highly enriched among 50-200bp mutations. To explore the relative impact of various mutational classes on crop fitness, we then track these structural events over the last century of US rice improvement using 101 resequenced varieties. Within this material, a pattern of temporary hybridization between medium and long-grain varieties was followed by recent divergence. During this long-term selection, structural mutations that impact gene exons have been removed at a greater rate than intronic indels and single-nucleotide mutations. These results support the use of ab initio estimates of mutational burden, based on structural data, as an orthogonal predictor in genomic selection.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009389&type=printable
spellingShingle Justin N Vaughn
Walid Korani
Joshua C Stein
Jeremy D Edwards
Daniel G Peterson
Sheron A Simpson
Ramey C Youngblood
Jane Grimwood
Kapeel Chougule
Doreen H Ware
Anna M McClung
Brian E Scheffler
Gene disruption by structural mutations drives selection in US rice breeding over the last century.
PLoS Genetics
title Gene disruption by structural mutations drives selection in US rice breeding over the last century.
title_full Gene disruption by structural mutations drives selection in US rice breeding over the last century.
title_fullStr Gene disruption by structural mutations drives selection in US rice breeding over the last century.
title_full_unstemmed Gene disruption by structural mutations drives selection in US rice breeding over the last century.
title_short Gene disruption by structural mutations drives selection in US rice breeding over the last century.
title_sort gene disruption by structural mutations drives selection in us rice breeding over the last century
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009389&type=printable
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