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...
Main Authors: | , , , , , , , , |
---|---|
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 |
_version_ | 1818506074283573248 |
---|---|
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. |
first_indexed | 2024-12-10T21:59:34Z |
format | Article |
id | doaj.art-aa5d83abbf2c422dbc65754e59d05684 |
institution | Directory Open Access Journal |
issn | 1664-462X |
language | English |
last_indexed | 2024-12-10T21:59:34Z |
publishDate | 2020-02-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Plant Science |
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 |
work_keys_str_mv | AT michaelahardigan genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT mitchelljfeldmann genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT annelorant genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT kevinabird genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT randifamula genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT charlotteacharya genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT glenncole genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT patrickpedger genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution AT stevenjknapp genomesyntenyhasbeenconservedamongtheoctoploidprogenitorsofcultivatedstrawberryovermillionsofyearsofevolution |