Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution

Allo-octoploid cultivated strawberry (Fragaria × ananassa) originated through a combination of polyploid and homoploid hybridization, domestication of an interspecific hybrid lineage, and continued admixture of wild species over the last 300 years. While genes appear to flow freely between the octop...

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Main Authors: Michael A. Hardigan, Mitchell J. Feldmann, Anne Lorant, Kevin A. Bird, Randi Famula, Charlotte Acharya, Glenn Cole, Patrick P. Edger, Steven J. Knapp
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.01789/full
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author Michael A. Hardigan
Mitchell J. Feldmann
Anne Lorant
Kevin A. Bird
Randi Famula
Charlotte Acharya
Glenn Cole
Patrick P. Edger
Steven J. Knapp
author_facet Michael A. Hardigan
Mitchell J. Feldmann
Anne Lorant
Kevin A. Bird
Randi Famula
Charlotte Acharya
Glenn Cole
Patrick P. Edger
Steven J. Knapp
author_sort Michael A. Hardigan
collection DOAJ
description Allo-octoploid cultivated strawberry (Fragaria × ananassa) originated through a combination of polyploid and homoploid hybridization, domestication of an interspecific hybrid lineage, and continued admixture of wild species over the last 300 years. While genes appear to flow freely between the octoploid progenitors, the genome structures and diversity of the octoploid species remain poorly understood. The complexity and absence of an octoploid genome frustrated early efforts to study chromosome evolution, resolve subgenomic structure, and develop a single coherent linkage group nomenclature. Here, we show that octoploid Fragaria species harbor millions of subgenome-specific DNA variants. Their diversity was sufficient to distinguish duplicated (homoeologous and paralogous) DNA sequences and develop 50K and 850K SNP genotyping arrays populated with co-dominant, disomic SNP markers distributed throughout the octoploid genome. Whole-genome shotgun genotyping of an interspecific segregating population yielded 1.9M genetically mapped subgenome variants in 5,521 haploblocks spanning 3,394 cM in F. chiloensis subsp. lucida, and 1.6M genetically mapped subgenome variants in 3,179 haploblocks spanning 2,017 cM in F. × ananassa. These studies provide a dense genomic framework of subgenome-specific DNA markers for seamlessly cross-referencing genetic and physical mapping information and unifying existing chromosome nomenclatures. Using comparative genomics, we show that geographically diverse wild octoploids are effectively diploidized, nearly completely collinear, and retain strong macro-synteny with diploid progenitor species. The preservation of genome structure among allo-octoploid taxa is a critical factor in the unique history of garden strawberry, where unimpeded gene flow supported its origin and domestication through repeated cycles of interspecific hybridization.
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spelling doaj.art-aa5d83abbf2c422dbc65754e59d056842022-12-22T01:31:57ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-02-011010.3389/fpls.2019.01789504896Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of EvolutionMichael A. Hardigan0Mitchell J. Feldmann1Anne Lorant2Kevin A. Bird3Randi Famula4Charlotte Acharya5Glenn Cole6Patrick P. Edger7Steven J. Knapp8Department of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Horticulture, Michigan State University, East Lansing, MI, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesDepartment of Horticulture, Michigan State University, East Lansing, MI, United StatesDepartment of Plant Sciences, University of California, Davis, Davis, CA, United StatesAllo-octoploid cultivated strawberry (Fragaria × ananassa) originated through a combination of polyploid and homoploid hybridization, domestication of an interspecific hybrid lineage, and continued admixture of wild species over the last 300 years. While genes appear to flow freely between the octoploid progenitors, the genome structures and diversity of the octoploid species remain poorly understood. The complexity and absence of an octoploid genome frustrated early efforts to study chromosome evolution, resolve subgenomic structure, and develop a single coherent linkage group nomenclature. Here, we show that octoploid Fragaria species harbor millions of subgenome-specific DNA variants. Their diversity was sufficient to distinguish duplicated (homoeologous and paralogous) DNA sequences and develop 50K and 850K SNP genotyping arrays populated with co-dominant, disomic SNP markers distributed throughout the octoploid genome. Whole-genome shotgun genotyping of an interspecific segregating population yielded 1.9M genetically mapped subgenome variants in 5,521 haploblocks spanning 3,394 cM in F. chiloensis subsp. lucida, and 1.6M genetically mapped subgenome variants in 3,179 haploblocks spanning 2,017 cM in F. × ananassa. These studies provide a dense genomic framework of subgenome-specific DNA markers for seamlessly cross-referencing genetic and physical mapping information and unifying existing chromosome nomenclatures. Using comparative genomics, we show that geographically diverse wild octoploids are effectively diploidized, nearly completely collinear, and retain strong macro-synteny with diploid progenitor species. The preservation of genome structure among allo-octoploid taxa is a critical factor in the unique history of garden strawberry, where unimpeded gene flow supported its origin and domestication through repeated cycles of interspecific hybridization.https://www.frontiersin.org/article/10.3389/fpls.2019.01789/fullFragariastrawberrypolyploidygenome evolutiondomestication
spellingShingle Michael A. Hardigan
Mitchell J. Feldmann
Anne Lorant
Kevin A. Bird
Randi Famula
Charlotte Acharya
Glenn Cole
Patrick P. Edger
Steven J. Knapp
Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution
Frontiers in Plant Science
Fragaria
strawberry
polyploidy
genome evolution
domestication
title Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution
title_full Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution
title_fullStr Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution
title_full_unstemmed Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution
title_short Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution
title_sort genome synteny has been conserved among the octoploid progenitors of cultivated strawberry over millions of years of evolution
topic Fragaria
strawberry
polyploidy
genome evolution
domestication
url https://www.frontiersin.org/article/10.3389/fpls.2019.01789/full
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