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      Chromosome Replacement and Deletion Lead to Clonal Polymorphism of Berry Color in Grapevine

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          Abstract

          Clonal polymorphism mainly results from somatic mutations that occur naturally during plant growth. In grapevine, arrays of clones have been selected within varieties as a valuable source of diversity, among them clones showing berry color polymorphism. To identify mutations responsible for this color polymorphism, we studied a collection of 33 clones of Pinot noir, Pinot gris, and Pinot blanc. Haplotypes of the L2 cell layer of nine clones were resolved by genotyping self-progenies with molecular markers along a 10.07 Mb region of chromosome 2, including the color locus. We demonstrated that at least six haplotypes could account for the loss of anthocyanin biosynthesis. Four of them resulted from the replacement of sections of the ‘colored’ haplotype, sized from 31 kb to 4.4 Mb, by the homologous sections of the ‘white’ haplotype mutated at the color locus. This transfer of information between the two homologous sequences resulted in the partial homozygosity of chromosome 2, associated in one case with a large deletion of 108 kb-long. Moreover, we showed that, in most cases, somatic mutations do not affect the whole plant; instead, they affect only one cell layer, leading to periclinal chimeras associating two genotypes. Analysis of bud sports of Pinot gris support the hypothesis that cell layer rearrangements in the chimera lead to the homogenization of the genotype in the whole plant. Our findings shed new light on the way molecular and cellular mechanisms shape the grapevine genotypes during vegetative propagation, and enable us to propose a scheme of evolutionary mechanism of the Pinot clones.

          Author Summary

          Pinot is one of the most ancient grapevine varieties made up of a large panel of clones, most of them used to produce very different wines with specific oenological characteristics in different vineyards around the world. This great diversity of clones, which is due to spontaneous somatic mutations that have occurred over time, makes Pinot a fascinating subject of study. It is the reason why we have undertaken a study focused on the color locus to identify the mutations responsible for color variation in a large panel of Pinot gris and Pinot blanc clones. The results we obtained shed light on large-scale molecular events that account for the loss of anthocyanin biosynthesis, such as chromosome replacement and deletion. These mutations first multiplied and, depending on the cell layer in which they occurred, lead to chimeras. Occasionally, cell layer rearrangements homogenize the whole plant. Clonal polymorphism of grapevine varieties results from a succession of such molecular and cellular mechanisms that are the driving forces behind the genetic drift of clones and the evolution of the grapevine genome.

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          The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla.

          The analysis of the first plant genomes provided unexpected evidence for genome duplication events in species that had previously been considered as true diploids on the basis of their genetics. These polyploidization events may have had important consequences in plant evolution, in particular for species radiation and adaptation and for the modulation of functional capacities. Here we report a high-quality draft of the genome sequence of grapevine (Vitis vinifera) obtained from a highly homozygous genotype. The draft sequence of the grapevine genome is the fourth one produced so far for flowering plants, the second for a woody species and the first for a fruit crop (cultivated for both fruit and beverage). Grapevine was selected because of its important place in the cultural heritage of humanity beginning during the Neolithic period. Several large expansions of gene families with roles in aromatic features are observed. The grapevine genome has not undergone recent genome duplication, thus enabling the discovery of ancestral traits and features of the genetic organization of flowering plants. This analysis reveals the contribution of three ancestral genomes to the grapevine haploid content. This ancestral arrangement is common to many dicotyledonous plants but is absent from the genome of rice, which is a monocotyledon. Furthermore, we explain the chronology of previously described whole-genome duplication events in the evolution of flowering plants.
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            A High Quality Draft Consensus Sequence of the Genome of a Heterozygous Grapevine Variety

            Background Worldwide, grapes and their derived products have a large market. The cultivated grape species Vitis vinifera has potential to become a model for fruit trees genetics. Like many plant species, it is highly heterozygous, which is an additional challenge to modern whole genome shotgun sequencing. In this paper a high quality draft genome sequence of a cultivated clone of V. vinifera Pinot Noir is presented. Principal Findings We estimate the genome size of V. vinifera to be 504.6 Mb. Genomic sequences corresponding to 477.1 Mb were assembled in 2,093 metacontigs and 435.1 Mb were anchored to the 19 linkage groups (LGs). The number of predicted genes is 29,585, of which 96.1% were assigned to LGs. This assembly of the grape genome provides candidate genes implicated in traits relevant to grapevine cultivation, such as those influencing wine quality, via secondary metabolites, and those connected with the extreme susceptibility of grape to pathogens. Single nucleotide polymorphism (SNP) distribution was consistent with a diffuse haplotype structure across the genome. Of around 2,000,000 SNPs, 1,751,176 were mapped to chromosomes and one or more of them were identified in 86.7% of anchored genes. The relative age of grape duplicated genes was estimated and this made possible to reveal a relatively recent Vitis-specific large scale duplication event concerning at least 10 chromosomes (duplication not reported before). Conclusions Sanger shotgun sequencing and highly efficient sequencing by synthesis (SBS), together with dedicated assembly programs, resolved a complex heterozygous genome. A consensus sequence of the genome and a set of mapped marker loci were generated. Homologous chromosomes of Pinot Noir differ by 11.2% of their DNA (hemizygous DNA plus chromosomal gaps). SNP markers are offered as a tool with the potential of introducing a new era in the molecular breeding of grape.
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              Retrotransposon-induced mutations in grape skin color.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                2 April 2015
                April 2015
                : 11
                : 4
                : e1005081
                Affiliations
                [1 ]INRA, UMR1131, Colmar, France
                [2 ]Université de Strasbourg, UMR1131, Strasbourg, France
                MicroTrek Incorporated, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: FP DM. Performed the experiments: FP VD LB SH. Analyzed the data: FP SH DM. Contributed reagents/materials/analysis tools: FP VD. Wrote the paper: FP DM.

                Article
                PGENETICS-D-14-02993
                10.1371/journal.pgen.1005081
                4383506
                25835388
                921c9c2a-2e88-49da-a7fc-270db85a9700
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 6 November 2014
                : 18 February 2015
                Page count
                Figures: 4, Tables: 2, Pages: 18
                Funding
                SH was a doctoral fellow funded by the Conseil Régional d’Alsace. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Genetics
                Genetics

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