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

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          Abstract

          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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          Evolution of crop species: genetics of domestication and diversification.

          Domestication is a good model for the study of evolutionary processes because of the recent evolution of crop species (<12,000 years ago), the key role of selection in their origins, and good archaeological and historical data on their spread and diversification. Recent studies, such as quantitative trait locus mapping, genome-wide association studies and whole-genome resequencing studies, have identified genes that are associated with the initial domestication and subsequent diversification of crops. Together, these studies reveal the functions of genes that are involved in the evolution of crops that are under domestication, the types of mutations that occur during this process and the parallelism of mutations that occur in the same pathways and proteins, as well as the selective forces that are acting on these mutations and that are associated with geographical adaptation of crop species.
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            High-throughput genotyping by whole-genome resequencing.

            The next-generation sequencing technology coupled with the growing number of genome sequences opens the opportunity to redesign genotyping strategies for more effective genetic mapping and genome analysis. We have developed a high-throughput method for genotyping recombinant populations utilizing whole-genome resequencing data generated by the Illumina Genome Analyzer. A sliding window approach is designed to collectively examine genome-wide single nucleotide polymorphisms for genotype calling and recombination breakpoint determination. Using this method, we constructed a genetic map for 150 rice recombinant inbred lines with an expected genotype calling accuracy of 99.94% and a resolution of recombination breakpoints within an average of 40 kb. In comparison to the genetic map constructed with 287 PCR-based markers for the rice population, the sequencing-based method was approximately 20x faster in data collection and 35x more precise in recombination breakpoint determination. Using the sequencing-based genetic map, we located a quantitative trait locus of large effect on plant height in a 100-kb region containing the rice "green revolution" gene. Through computer simulation, we demonstrate that the method is robust for different types of mapping populations derived from organisms with variable quality of genome sequences and is feasible for organisms with large genome sizes and low polymorphisms. With continuous advances in sequencing technologies, this genome-based method may replace the conventional marker-based genotyping approach to provide a powerful tool for large-scale gene discovery and for addressing a wide range of biological questions.
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              HYBRID ORIGINS OF PLANT SPECIES

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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                07 February 2020
                2019
                : 10
                : 1789
                Affiliations
                [1] 1 Department of Plant Sciences, University of California, Davis , Davis, CA, United States
                [2] 2 Department of Horticulture, Michigan State University , East Lansing, MI, United States
                Author notes

                Edited by: Martin A. Lysak, Masaryk University, Czechia

                Reviewed by: Martin Mascher, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Germany; Yongpeng Ma, Chinese Academy of Sciences, China

                *Correspondence: Steven J. Knapp, sjknapp@ 123456ucdavis.edu

                This article was submitted to Plant Systematics and Evolution, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.01789
                7020885
                32158449
                892d2cd5-b44f-48d1-800b-036717479cf8
                Copyright © 2020 Hardigan, Feldmann, Lorant, Bird, Famula, Acharya, Cole, Edger and Knapp

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 17 October 2019
                : 20 December 2019
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 97, Pages: 17, Words: 8537
                Funding
                Funded by: U.S. Department of Agriculture 10.13039/100000199
                Award ID: 2017-51181-26833, 2018-67012-27980
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                fragaria,strawberry,polyploidy,genome evolution,domestication
                Plant science & Botany
                fragaria, strawberry, polyploidy, genome evolution, domestication

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