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Chromosome replacement and deletion lead to clonal polymorphism of berry color in grapevine.

Pelsy F, Dumas V, Bévilacqua L, Hocquigny S, Merdinoglu D - PLoS Genet. (2015)

Bottom Line: Clonal polymorphism mainly results from somatic mutations that occur naturally during plant growth.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.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR1131, Colmar, France; Université de Strasbourg, UMR1131, Strasbourg, France.

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.

No MeSH data available.


Related in: MedlinePlus

Models for pathways proposed to explain the non-canonical ‘white’ haplotypes.These models are based on the repair of DSBs. After induction of the double-strand break in the acceptor molecule, in that case the ‘colored’ haplotype (solid black line), the ends are processing to yield 3’single-strands tails. Then, the 3’ends invades the double-stranded donor molecule, here the ‘white’ haplotype (solid grey line) and repair synthesis occurs. For the further processing of the intermediate two possible outcomes can be envisaged. For the formation of w188-1: the acceptor molecule is elongating, possibly up to the homology of the second 3’end of the DSB followed by the insertion of a genomic sequence copied from elsewhere into the break. For the formation of w188-2: the acceptor molecule is elongating up to the end of the chromosome using the invading donor sequence as template.
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pgen.1005081.g003: Models for pathways proposed to explain the non-canonical ‘white’ haplotypes.These models are based on the repair of DSBs. After induction of the double-strand break in the acceptor molecule, in that case the ‘colored’ haplotype (solid black line), the ends are processing to yield 3’single-strands tails. Then, the 3’ends invades the double-stranded donor molecule, here the ‘white’ haplotype (solid grey line) and repair synthesis occurs. For the further processing of the intermediate two possible outcomes can be envisaged. For the formation of w188-1: the acceptor molecule is elongating, possibly up to the homology of the second 3’end of the DSB followed by the insertion of a genomic sequence copied from elsewhere into the break. For the formation of w188-2: the acceptor molecule is elongating up to the end of the chromosome using the invading donor sequence as template.

Mentions: The non-canonical ‘white’ haplotypes consisting in the replacement of a more or less extended section of the ‘colored’ haplotype by the ‘white’ haplotype could have been generated by gene conversion which represents the non-reciprocal transfer of information between two homologous sequences to duplicate one of the haplotype, with the corresponding loss of the other [35]. Gene conversion operates during replicative DNA synthesis and is well documented in yeast [36], rice [37] as well as in human [38]. The model of recombination starts by a double-strand break (DSB) in the recipient molecule, in our case the ‘colored’ haplotype (Fig. 3). Then, one end of the DSB invades the homologous chromosome, the ‘white’ haplotype, and repairs the break using the sequence of the homolog as template. The invading strand can reach the end of the chromosome replacing the recipient molecule by the donor sequence. Such a mechanism can explain haplotype w188-2. If the process stops before the end of the chromosome, it results in a loss of information on the recipient haplotype as in the case of haplotype w188-3, truncated beyond marker VVIu20.1. The extension of the molecule can also stop before the end of the chromosome where the recipient sequence is recovered. Such a mechanism can explain the probable non-canonical ‘white’ haplotype giving the particular genotypes of the white bud sports and of the L2 cell layer of their grey parents.


Chromosome replacement and deletion lead to clonal polymorphism of berry color in grapevine.

Pelsy F, Dumas V, Bévilacqua L, Hocquigny S, Merdinoglu D - PLoS Genet. (2015)

Models for pathways proposed to explain the non-canonical ‘white’ haplotypes.These models are based on the repair of DSBs. After induction of the double-strand break in the acceptor molecule, in that case the ‘colored’ haplotype (solid black line), the ends are processing to yield 3’single-strands tails. Then, the 3’ends invades the double-stranded donor molecule, here the ‘white’ haplotype (solid grey line) and repair synthesis occurs. For the further processing of the intermediate two possible outcomes can be envisaged. For the formation of w188-1: the acceptor molecule is elongating, possibly up to the homology of the second 3’end of the DSB followed by the insertion of a genomic sequence copied from elsewhere into the break. For the formation of w188-2: the acceptor molecule is elongating up to the end of the chromosome using the invading donor sequence as template.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4383506&req=5

pgen.1005081.g003: Models for pathways proposed to explain the non-canonical ‘white’ haplotypes.These models are based on the repair of DSBs. After induction of the double-strand break in the acceptor molecule, in that case the ‘colored’ haplotype (solid black line), the ends are processing to yield 3’single-strands tails. Then, the 3’ends invades the double-stranded donor molecule, here the ‘white’ haplotype (solid grey line) and repair synthesis occurs. For the further processing of the intermediate two possible outcomes can be envisaged. For the formation of w188-1: the acceptor molecule is elongating, possibly up to the homology of the second 3’end of the DSB followed by the insertion of a genomic sequence copied from elsewhere into the break. For the formation of w188-2: the acceptor molecule is elongating up to the end of the chromosome using the invading donor sequence as template.
Mentions: The non-canonical ‘white’ haplotypes consisting in the replacement of a more or less extended section of the ‘colored’ haplotype by the ‘white’ haplotype could have been generated by gene conversion which represents the non-reciprocal transfer of information between two homologous sequences to duplicate one of the haplotype, with the corresponding loss of the other [35]. Gene conversion operates during replicative DNA synthesis and is well documented in yeast [36], rice [37] as well as in human [38]. The model of recombination starts by a double-strand break (DSB) in the recipient molecule, in our case the ‘colored’ haplotype (Fig. 3). Then, one end of the DSB invades the homologous chromosome, the ‘white’ haplotype, and repairs the break using the sequence of the homolog as template. The invading strand can reach the end of the chromosome replacing the recipient molecule by the donor sequence. Such a mechanism can explain haplotype w188-2. If the process stops before the end of the chromosome, it results in a loss of information on the recipient haplotype as in the case of haplotype w188-3, truncated beyond marker VVIu20.1. The extension of the molecule can also stop before the end of the chromosome where the recipient sequence is recovered. Such a mechanism can explain the probable non-canonical ‘white’ haplotype giving the particular genotypes of the white bud sports and of the L2 cell layer of their grey parents.

Bottom Line: Clonal polymorphism mainly results from somatic mutations that occur naturally during plant growth.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.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR1131, Colmar, France; Université de Strasbourg, UMR1131, Strasbourg, France.

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.

No MeSH data available.


Related in: MedlinePlus