Limits...
A haplotype map of allohexaploid wheat reveals distinct patterns of selection on homoeologous genomes.

Jordan KW, Wang S, Lun Y, Gardiner LJ, MacLachlan R, Hucl P, Wiebe K, Wong D, Forrest KL, IWGS ConsortiumSharpe AG, Sidebottom CH, Hall N, Toomajian C, Close T, Dubcovsky J, Akhunova A, Talbert L, Bansal UK, Bariana HS, Hayden MJ, Pozniak C, Jeddeloh JA, Hall A, Akhunov E - Genome Biol. (2015)

Bottom Line: These selected regions are enriched for loci associated with agronomic traits detected in genome-wide association studies.Evidence suggests that directional selection in allopolyploids rarely acted on multiple parallel advantageous mutations across homoeologous regions, likely indicating that a fitness benefit could be obtained by a mutation at any one of the homoeologs.Additional advantageous variants in other homoelogs probably either contributed little benefit, or were unavailable in populations subjected to directional selection.

View Article: PubMed Central - PubMed

Affiliation: Department Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA. kwjordan@k-state.edu.

ABSTRACT

Background: Bread wheat is an allopolyploid species with a large, highly repetitive genome. To investigate the impact of selection on variants distributed among homoeologous wheat genomes and to build a foundation for understanding genotype-phenotype relationships, we performed population-scale re-sequencing of a diverse panel of wheat lines.

Results: A sample of 62 diverse lines was re-sequenced using the whole exome capture and genotyping-by-sequencing approaches. We describe the allele frequency, functional significance, and chromosomal distribution of 1.57 million single nucleotide polymorphisms and 161,719 small indels. Our results suggest that duplicated homoeologous genes are under purifying selection. We find contrasting patterns of variation and inter-variant associations among wheat genomes; this, in addition to demographic factors, could be explained by differences in the effect of directional selection on duplicated homoeologs. Only a small fraction of the homoeologous regions harboring selected variants overlapped among the wheat genomes in any given wheat line. These selected regions are enriched for loci associated with agronomic traits detected in genome-wide association studies.

Conclusions: Evidence suggests that directional selection in allopolyploids rarely acted on multiple parallel advantageous mutations across homoeologous regions, likely indicating that a fitness benefit could be obtained by a mutation at any one of the homoeologs. Additional advantageous variants in other homoelogs probably either contributed little benefit, or were unavailable in populations subjected to directional selection. We hypothesize that allopolyploidy may have increased the likelihood of beneficial allele recovery by broadening the set of possible selection targets.

Show MeSH
Distribution of genetic diversity, allele frequency, and recombination across the wheat genome. (a) Distribution of genetic diversity in the A (green), B (red), and D (blue) genomes: (π, top left), Tajima’s measure of site frequency spectrum (D, top right), historic recombination (ρ, bottom left), and LD (bottom right). (b) Distribution of nucleotide diversity π (shaded polygon), FST between cultivars and landraces (solid black line), and site frequency spectrum (D) along chromosomes 5A (top panel), 5B (middle panel) and 5D (bottom panel). Gray shaded boxes represent the approximate location of the centromere. Rug plots represent lower (red) and upper (blue) 2.5% tails of test statistic distribution. Black X above the plot represents upper 2.5% tail of ρ statistic. The location of domestication (Q) gene is shown by arrow. (c). Distribution of alleles of the AL8/78 genotype of Ae. tauschii along the chromosomes of the D genome in the 26 wheat landraces. The average frequency of AL8/78 alleles was calculated in a 3 Mb sliding window. The color scale shows the proportion of the AL8/78 alleles in each window (red - highest, blue - lowest).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4389885&req=5

Fig2: Distribution of genetic diversity, allele frequency, and recombination across the wheat genome. (a) Distribution of genetic diversity in the A (green), B (red), and D (blue) genomes: (π, top left), Tajima’s measure of site frequency spectrum (D, top right), historic recombination (ρ, bottom left), and LD (bottom right). (b) Distribution of nucleotide diversity π (shaded polygon), FST between cultivars and landraces (solid black line), and site frequency spectrum (D) along chromosomes 5A (top panel), 5B (middle panel) and 5D (bottom panel). Gray shaded boxes represent the approximate location of the centromere. Rug plots represent lower (red) and upper (blue) 2.5% tails of test statistic distribution. Black X above the plot represents upper 2.5% tail of ρ statistic. The location of domestication (Q) gene is shown by arrow. (c). Distribution of alleles of the AL8/78 genotype of Ae. tauschii along the chromosomes of the D genome in the 26 wheat landraces. The average frequency of AL8/78 alleles was calculated in a 3 Mb sliding window. The color scale shows the proportion of the AL8/78 alleles in each window (red - highest, blue - lowest).

Mentions: The global patterns of genomic variation and distribution of inter-variant associations are impacted by historic selection and demographic events, and by variation in recombination rate [40]. We found a non-random variant distribution along the chromosomes with reduced variation near the centromeres and elevated variation at the telomeres (Figure 2a and b; Figures S10-15 in Additional file 1), which is consistent with previous studies [28,30]. This pattern is similar to what was reported for maize and humans [19,41], but differs from Arabidopsis [37], where regions of high polymorphism were located near the centromeres. Our data also showed reduced diversity and an excess of rare alleles in the D genome when compared to the A and B genomes (Figure 2a; Table S9 in Additional file 1) [30]. These trends are consistent with the hypothesis that the limited number of ancestral genotypes of the D genome contributed to the origin of hexaploid wheat [42]. An elevated level of diversity in the A and B genomes, which otherwise would be expected to show the same levels of diversity as the D genome, could be attributed to the influx of allelic variation from the sympatric populations of wild tetraploid relatives [7,43].Figure 2


A haplotype map of allohexaploid wheat reveals distinct patterns of selection on homoeologous genomes.

Jordan KW, Wang S, Lun Y, Gardiner LJ, MacLachlan R, Hucl P, Wiebe K, Wong D, Forrest KL, IWGS ConsortiumSharpe AG, Sidebottom CH, Hall N, Toomajian C, Close T, Dubcovsky J, Akhunova A, Talbert L, Bansal UK, Bariana HS, Hayden MJ, Pozniak C, Jeddeloh JA, Hall A, Akhunov E - Genome Biol. (2015)

Distribution of genetic diversity, allele frequency, and recombination across the wheat genome. (a) Distribution of genetic diversity in the A (green), B (red), and D (blue) genomes: (π, top left), Tajima’s measure of site frequency spectrum (D, top right), historic recombination (ρ, bottom left), and LD (bottom right). (b) Distribution of nucleotide diversity π (shaded polygon), FST between cultivars and landraces (solid black line), and site frequency spectrum (D) along chromosomes 5A (top panel), 5B (middle panel) and 5D (bottom panel). Gray shaded boxes represent the approximate location of the centromere. Rug plots represent lower (red) and upper (blue) 2.5% tails of test statistic distribution. Black X above the plot represents upper 2.5% tail of ρ statistic. The location of domestication (Q) gene is shown by arrow. (c). Distribution of alleles of the AL8/78 genotype of Ae. tauschii along the chromosomes of the D genome in the 26 wheat landraces. The average frequency of AL8/78 alleles was calculated in a 3 Mb sliding window. The color scale shows the proportion of the AL8/78 alleles in each window (red - highest, blue - lowest).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4389885&req=5

Fig2: Distribution of genetic diversity, allele frequency, and recombination across the wheat genome. (a) Distribution of genetic diversity in the A (green), B (red), and D (blue) genomes: (π, top left), Tajima’s measure of site frequency spectrum (D, top right), historic recombination (ρ, bottom left), and LD (bottom right). (b) Distribution of nucleotide diversity π (shaded polygon), FST between cultivars and landraces (solid black line), and site frequency spectrum (D) along chromosomes 5A (top panel), 5B (middle panel) and 5D (bottom panel). Gray shaded boxes represent the approximate location of the centromere. Rug plots represent lower (red) and upper (blue) 2.5% tails of test statistic distribution. Black X above the plot represents upper 2.5% tail of ρ statistic. The location of domestication (Q) gene is shown by arrow. (c). Distribution of alleles of the AL8/78 genotype of Ae. tauschii along the chromosomes of the D genome in the 26 wheat landraces. The average frequency of AL8/78 alleles was calculated in a 3 Mb sliding window. The color scale shows the proportion of the AL8/78 alleles in each window (red - highest, blue - lowest).
Mentions: The global patterns of genomic variation and distribution of inter-variant associations are impacted by historic selection and demographic events, and by variation in recombination rate [40]. We found a non-random variant distribution along the chromosomes with reduced variation near the centromeres and elevated variation at the telomeres (Figure 2a and b; Figures S10-15 in Additional file 1), which is consistent with previous studies [28,30]. This pattern is similar to what was reported for maize and humans [19,41], but differs from Arabidopsis [37], where regions of high polymorphism were located near the centromeres. Our data also showed reduced diversity and an excess of rare alleles in the D genome when compared to the A and B genomes (Figure 2a; Table S9 in Additional file 1) [30]. These trends are consistent with the hypothesis that the limited number of ancestral genotypes of the D genome contributed to the origin of hexaploid wheat [42]. An elevated level of diversity in the A and B genomes, which otherwise would be expected to show the same levels of diversity as the D genome, could be attributed to the influx of allelic variation from the sympatric populations of wild tetraploid relatives [7,43].Figure 2

Bottom Line: These selected regions are enriched for loci associated with agronomic traits detected in genome-wide association studies.Evidence suggests that directional selection in allopolyploids rarely acted on multiple parallel advantageous mutations across homoeologous regions, likely indicating that a fitness benefit could be obtained by a mutation at any one of the homoeologs.Additional advantageous variants in other homoelogs probably either contributed little benefit, or were unavailable in populations subjected to directional selection.

View Article: PubMed Central - PubMed

Affiliation: Department Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA. kwjordan@k-state.edu.

ABSTRACT

Background: Bread wheat is an allopolyploid species with a large, highly repetitive genome. To investigate the impact of selection on variants distributed among homoeologous wheat genomes and to build a foundation for understanding genotype-phenotype relationships, we performed population-scale re-sequencing of a diverse panel of wheat lines.

Results: A sample of 62 diverse lines was re-sequenced using the whole exome capture and genotyping-by-sequencing approaches. We describe the allele frequency, functional significance, and chromosomal distribution of 1.57 million single nucleotide polymorphisms and 161,719 small indels. Our results suggest that duplicated homoeologous genes are under purifying selection. We find contrasting patterns of variation and inter-variant associations among wheat genomes; this, in addition to demographic factors, could be explained by differences in the effect of directional selection on duplicated homoeologs. Only a small fraction of the homoeologous regions harboring selected variants overlapped among the wheat genomes in any given wheat line. These selected regions are enriched for loci associated with agronomic traits detected in genome-wide association studies.

Conclusions: Evidence suggests that directional selection in allopolyploids rarely acted on multiple parallel advantageous mutations across homoeologous regions, likely indicating that a fitness benefit could be obtained by a mutation at any one of the homoeologs. Additional advantageous variants in other homoelogs probably either contributed little benefit, or were unavailable in populations subjected to directional selection. We hypothesize that allopolyploidy may have increased the likelihood of beneficial allele recovery by broadening the set of possible selection targets.

Show MeSH