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, 3 (6), 1003-13

Retrospective View of North American Potato (Solanum Tuberosum L.) Breeding in the 20th and 21st Centuries

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Retrospective View of North American Potato (Solanum Tuberosum L.) Breeding in the 20th and 21st Centuries

Candice N Hirsch et al. G3 (Bethesda).

Abstract

Cultivated potato (Solanum tuberosum L.), a vegetatively propagated autotetraploid, has been bred for distinct market classes, including fresh market, pigmented, and processing varieties. Breeding efforts have relied on phenotypic selection of populations developed from intra- and intermarket class crosses and introgressions of wild and cultivated Solanum relatives. To retrospectively explore the effects of potato breeding at the genome level, we used 8303 single-nucleotide polymorphism markers to genotype a 250-line diversity panel composed of wild species, genetic stocks, and cultivated potato lines with release dates ranging from 1857 to 2011. Population structure analysis revealed four subpopulations within the panel, with cultivated potato lines grouping together and separate from wild species and genetic stocks. With pairwise kinship estimates clear separation between potato market classes was observed. Modern breeding efforts have scarcely changed the percentage of heterozygous loci or the frequency of homozygous, single-dose, and duplex loci on a genome level, despite concerted efforts by breeders. In contrast, clear selection in less than 50 years of breeding was observed for alleles in biosynthetic pathways important for market class-specific traits such as pigmentation and carbohydrate composition. Although improvement and diversification for distinct market classes was observed through whole-genome analysis of historic and current potato lines, an increased rate of gain from selection will be required to meet growing global food demands and challenges due to climate change. Understanding the genetic basis of diversification and trait improvement will allow for more rapid genome-guided improvement of potato in future breeding efforts.

Keywords: Solanum tuberosum; genomics; genotypic diversity; phenotypic diversity.

Figures

Figure 1
Figure 1
Phenotypic and geographic diversity represented within the diversity panel. (A) Representative lines from each of the market classes (I. French Fry Processing, II. Table Russet, III. Chip Processing, IV. Round White Table, V. Yellow, VI. Pigmented (red skin with white flesh), VII. Pigmented (purple skin with purple flesh), and VIII. Genetic Stock). Geographic distribution within the United States (B) and worldwide (C) are based on breeding program from which the line was released and collection location. Blue shading indicates U.S. states that are represented in the diversity panel, red shading indicates countries that are represented in the diversity panel, and yellow shading indicates states or countries that are not represented in the diversity panel.
Figure 2
Figure 2
Genetic structure and divergence between market classes. (A) Graphical display of population substructure for 250 lines based on 6373 SNP markers using the diploid genotype calls with K = 4 populations. Population substructure was determined using STRUCTURE (Pritchard et al. 2000). Each vertical bar represents one individual in the population and each individual is partitioned into the four possible subpopulations based on the percentage of membership in each subpopulation. Subpopulation 1: red (30/41 with majority membership Chip Processing); subpopulation 2: green (7/8 with majority membership Genetic Stock); subpopulation 3: blue (157/160 with majority membership cultivated potato); subpopulation 4: yellow (19/19 with majority membership wild species or genetic stock)). (B) Unweighted pair group method with arithmetic mean (UPGMA) tree of 250 potato lines based on 3763 SNP markers with dosage genotype calls. Color-coding is based on predominant market class designation and asterisks indicate lines that can be classified into more than one market class (red: Chip Processing; dark blue: Genetic Stock; purple: Pigmented; green: French Fry Processing; light blue: Round White Table; pink: wild species; brown: Table Russet; yellow: Yellow).
Figure 3
Figure 3
Percent heterozygosity and allele dosage frequency distributions. Percent heterozygosity was determined with 6373 SNP markers and a diploid genotyping model. Allele dosage frequencies were determined with 3763 SNP markers and a dosage genotyping model. (A) Distribution of percent heterozygosity across the 250 lines in the diversity panel. (B) Histogram of percent heterozygosity in cultivated potato vs. all of the wild species and genetic stocks. (C) Histogram of percent heterozygosity in diploid vs. tetraploid lines. (D) Percent heterozygosity in wild species individuals. (E) Distribution of average percent allele dosage frequencies within each market classes for tetraploid lines only. (F) Proportion of allele dosage frequencies within individual released lines by release year for tetraploid lines only.
Figure 4
Figure 4
Selection for carotenoid biosynthetic pathway genes in Yellow fleshed market class potato lines. SNPs located within carotenoid biosynthetic pathway genes were tested for significant differences in allele or genotype composition compared to that observed in all other cultivated potato lines, and only SNPs that had a P < 0.05 for either genotype or allele frequencies are shown. In some cases, a SNP was only significant at either the genotype or allele level. Orange bars indicate percent of the Yellow lines with a given genotype, and aqua bars indicate percent of all other cultivated tetraploid potato lines. Blue and red bars indicate the percent of A and B alleles, respectively. PDS, phytoene dehydrogenase; ZDS, zeta-carotene desaturase; LCY-e, lycopene epsilon cyclase; LCY-b, lycopene beta cyclase; CHY1, beta-carotene hydroxylase 1.
Figure 5
Figure 5
Effect of phenotypic selection on market class divergence and overall species improvement over a century of potato breeding. Phenotypic traits were evaluated in three total replications in 2010 across two locations (New York and Wisconsin). (A) Scatter plot of least square means by release year for 31 potato chip lines that have been released between 1962 and 2011. Low snack food association chip color corresponds to lighter chip color, and 2.0 is considered acceptable by the potato chip industry. (B) Scatter plot of least square means by release year for the 115 lines in the diversity panel that have been released between 1857 and 2011. Lines are color-coded based on market class (Chip Processing: red, French Fry Processing: green, Pigmented: purple, Round White Table: light blue, Table Russet: brown, and Yellow: yellow). The black arrow is pointing to La Chipper. (C and D) Scatter plots of least square means by release year for 31 potato chip lines that have been released between 1962 and 2011.
Figure 6
Figure 6
Selection for carbohydrate synthesis, degradation, transport, and regulatory genes in Chip Processing clones. SNPs within 25 genes were tested for significant differences in allele and genotype composition between Chip Processing clones and all other cultivated potato [(A) allele, (B) genotype] and between French Fry Processing clones and non-processing cultivated potato clones [Pigmented, Round White Table, Table Russet, Yellow; (C) allele, (D) genotype]. The x-axis in all graphs is the position on each of the 12 potato chromosomes and the y-axis is a –log10 transformation of the P-value for the χ2 tests. Blue data points are SNPs in carbohydrate degradation genes, red data points are SNPs in carbohydrate synthesis genes, yellow data points are SNPs in carbohydrate transport genes, and the purple data point is a SNP in a regulatory gene annotated as invertase inhibitor. The data points with an x behind them are the most significant SNP within a gene. The black horizontal lines indicate significance at P = 0.05 and the gray lines at P = 0.01.

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