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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

Schematic presentation of the Pinot haplotypes determined by genetic analysis.Solid grey line corresponds to the ‘white’ haplotype and solid black line to the ‘colored’ haplotype. Dotted lines symbolize deletion or unknown sequences. The boxes represent VvmybA genes: A1: VvmybA1 and A2: VvmybA2. The grey triangle indicates the insertion. Positions on chromosome 2 are given en Mb according to the 12X genome sequence.
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pgen.1005081.g002: Schematic presentation of the Pinot haplotypes determined by genetic analysis.Solid grey line corresponds to the ‘white’ haplotype and solid black line to the ‘colored’ haplotype. Dotted lines symbolize deletion or unknown sequences. The boxes represent VvmybA genes: A1: VvmybA1 and A2: VvmybA2. The grey triangle indicates the insertion. Positions on chromosome 2 are given en Mb according to the 12X genome sequence.

Mentions: In the same way, haplotypes of eight clones were determined in their self-progenies, comprising 18 or 24 individuals. The selected clones were the following: three grey-skinned clones, PG52 and PG53 (genotype I) and PG3106 (genotype III) and five green-yellow-skinned clones, PB54 and PB55 (genotype IV), PB3009 and PB3172 (genotype V) and PB3232 (genotype VIII). As only the genetic information of the L2 cell layer is transmitted through sexual reproduction, only the haplotypes of the L2 cell layer could be determined. In the self-progeny of PG52, both alleles of loci from VMC5g7 to P2-442 displayed the expected Mendelian inheritance as well as those beyond VVNTm3, unlike alleles 168 at VVNTm1, 387 at VVNTm2, and VvMybA2 displaying the 2-bp deletion (CA) that were shown by all siblings. Conversely, amplification of the full site of Gret1 segregated and siblings that did not amplified the Gret1 insertion specifically displayed alleles belonging to haplotype c188 upstream from P2-442 and downstream from VVNTm3. In addition, the empty site of Gret1 was never amplified in these siblings. From this data, it was deduced that PG52 associated the canonical ‘white’ haplotype w216 and a new ‘white’ haplotype, w188-1, that displayed all alleles of canonical ‘colored’ haplotype c188, except alleles 168 at VVNTm1, 387 at VVNTm2 and VvMybA2 displaying the 2-bp deletion (CA) that were those of the ‘white’ haplotype w216 and lacked the Gret1 insertion. The four progenies of PG3106, PB54, PB55 and PB3232 showed the same Mendelian inheritance as PG52, except for VMC5g7 that segregated alleles 188 and 198, thus associating another ‘white’ haplotype w198 and the non-canonical ‘white’ haplotype, w188-1. Although the ‘white’ haplotypes w216 and w198 had different alleles at locus VMC5g7, both were considered as canonical ‘white’ haplotypes because they were identical at all other loci from SC8_0146_01 to VMC7g3. Conversely, in self-progenies of PB3009 and PB3172 all siblings displayed alleles belonging to w216 at all loci from P2-442 to VMC7g3 without segregation, including the Gret1 full site, while they displayed a Mendelian inheritance for loci upstream from P2-298. The self-progeny of PG53 differed from the previous one by the segregation of allele 116 at VMC7g3 that was not amplified in 22% of the progeny. From this data, two additional non-canonical ‘white’ haplotypes were deduced, w188-2 and w188-3, that displayed alleles belonging to c188 from VMC5g7 to P-298 and alleles belonging to w216 (or w198) from P2-442 to VMC7g3, except haplotype w188-3 that had a allele at VMC7g3 (Fig. 2).


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)

Schematic presentation of the Pinot haplotypes determined by genetic analysis.Solid grey line corresponds to the ‘white’ haplotype and solid black line to the ‘colored’ haplotype. Dotted lines symbolize deletion or unknown sequences. The boxes represent VvmybA genes: A1: VvmybA1 and A2: VvmybA2. The grey triangle indicates the insertion. Positions on chromosome 2 are given en Mb according to the 12X genome sequence.
© Copyright Policy
Related In: Results  -  Collection

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

pgen.1005081.g002: Schematic presentation of the Pinot haplotypes determined by genetic analysis.Solid grey line corresponds to the ‘white’ haplotype and solid black line to the ‘colored’ haplotype. Dotted lines symbolize deletion or unknown sequences. The boxes represent VvmybA genes: A1: VvmybA1 and A2: VvmybA2. The grey triangle indicates the insertion. Positions on chromosome 2 are given en Mb according to the 12X genome sequence.
Mentions: In the same way, haplotypes of eight clones were determined in their self-progenies, comprising 18 or 24 individuals. The selected clones were the following: three grey-skinned clones, PG52 and PG53 (genotype I) and PG3106 (genotype III) and five green-yellow-skinned clones, PB54 and PB55 (genotype IV), PB3009 and PB3172 (genotype V) and PB3232 (genotype VIII). As only the genetic information of the L2 cell layer is transmitted through sexual reproduction, only the haplotypes of the L2 cell layer could be determined. In the self-progeny of PG52, both alleles of loci from VMC5g7 to P2-442 displayed the expected Mendelian inheritance as well as those beyond VVNTm3, unlike alleles 168 at VVNTm1, 387 at VVNTm2, and VvMybA2 displaying the 2-bp deletion (CA) that were shown by all siblings. Conversely, amplification of the full site of Gret1 segregated and siblings that did not amplified the Gret1 insertion specifically displayed alleles belonging to haplotype c188 upstream from P2-442 and downstream from VVNTm3. In addition, the empty site of Gret1 was never amplified in these siblings. From this data, it was deduced that PG52 associated the canonical ‘white’ haplotype w216 and a new ‘white’ haplotype, w188-1, that displayed all alleles of canonical ‘colored’ haplotype c188, except alleles 168 at VVNTm1, 387 at VVNTm2 and VvMybA2 displaying the 2-bp deletion (CA) that were those of the ‘white’ haplotype w216 and lacked the Gret1 insertion. The four progenies of PG3106, PB54, PB55 and PB3232 showed the same Mendelian inheritance as PG52, except for VMC5g7 that segregated alleles 188 and 198, thus associating another ‘white’ haplotype w198 and the non-canonical ‘white’ haplotype, w188-1. Although the ‘white’ haplotypes w216 and w198 had different alleles at locus VMC5g7, both were considered as canonical ‘white’ haplotypes because they were identical at all other loci from SC8_0146_01 to VMC7g3. Conversely, in self-progenies of PB3009 and PB3172 all siblings displayed alleles belonging to w216 at all loci from P2-442 to VMC7g3 without segregation, including the Gret1 full site, while they displayed a Mendelian inheritance for loci upstream from P2-298. The self-progeny of PG53 differed from the previous one by the segregation of allele 116 at VMC7g3 that was not amplified in 22% of the progeny. From this data, two additional non-canonical ‘white’ haplotypes were deduced, w188-2 and w188-3, that displayed alleles belonging to c188 from VMC5g7 to P-298 and alleles belonging to w216 (or w198) from P2-442 to VMC7g3, except haplotype w188-3 that had a allele at VMC7g3 (Fig. 2).

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