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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.

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Summary of re-sequencing panel. (a) Evolution of the hexaploid wheat genome. The tetraploid wheat T. turgidum (AABB) originated by the hybridization of T. urartu with the close unidentified relative of Ae. speltoides occurred about 0.58 to 0.82 million years ago according to the genome-wide divergence time estimate [10]. The origin of hexaploid wheat occurred about 10,000 years ago [11] by the hybridization of T. turgidum with Ae. tauschii (DD) [12]. Marcussen et al. [10] suggested that Ae. tauschii might have originated by homoploid hybrid speciation (shown by dashed arrows). (b) Geographic distribution of 62 accessions of wheat accessions. Pie charts indicate the proportion of genetic ancestry for K = 4 inferred using Structure. (c) Efficiency of homoeologous gene capture. The depth of read coverage was extracted for each of the three copies of 47,739 homoeologous gene sets. The histogram of the log2 transformed ratio of read coverage between A and B (red), A and D (blue), and B and D (green) genomes was plotted. Each plot shows a normal distribution with the overall mean at 0. (d) Overlap between the SNP and indel datasets generated by WEC and GBS. (e) Minor allele frequency of different functional classes of SNPs as a proportion of total SNPs within each genome and class. PTC: premature termination codons; SSD: splice-site disruptions.
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Fig1: Summary of re-sequencing panel. (a) Evolution of the hexaploid wheat genome. The tetraploid wheat T. turgidum (AABB) originated by the hybridization of T. urartu with the close unidentified relative of Ae. speltoides occurred about 0.58 to 0.82 million years ago according to the genome-wide divergence time estimate [10]. The origin of hexaploid wheat occurred about 10,000 years ago [11] by the hybridization of T. turgidum with Ae. tauschii (DD) [12]. Marcussen et al. [10] suggested that Ae. tauschii might have originated by homoploid hybrid speciation (shown by dashed arrows). (b) Geographic distribution of 62 accessions of wheat accessions. Pie charts indicate the proportion of genetic ancestry for K = 4 inferred using Structure. (c) Efficiency of homoeologous gene capture. The depth of read coverage was extracted for each of the three copies of 47,739 homoeologous gene sets. The histogram of the log2 transformed ratio of read coverage between A and B (red), A and D (blue), and B and D (green) genomes was plotted. Each plot shows a normal distribution with the overall mean at 0. (d) Overlap between the SNP and indel datasets generated by WEC and GBS. (e) Minor allele frequency of different functional classes of SNPs as a proportion of total SNPs within each genome and class. PTC: premature termination codons; SSD: splice-site disruptions.

Mentions: Wheat genomic variation is shaped by the interplay of multiple factors including two recent polyploidization events [1-3] (Figure 1a), domestication [4], spread from the sites of origin to new geographic regions, gene flow from the populations of wild and domesticated ancestors [5], and post-domestication selection aimed at developing high-yielding locally adapted varieties. The eco-geographic habitats to which wheat is adapted span diverse environments ranging from low humidity regions in Nigeria, and the northern regions of Russia and Norway to the high-humidity regions of South America and Bangladesh [6]. It has been suggested that this broad adaptability likely results from the genetic diversity captured from the natural populations of its tetraploid ancestors [5,7] combined with a high rate of evolutionary changes in the wheat genome (particularly insertions and deletions), which are tolerated by its polyploid nature [8,9].Figure 1


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)

Summary of re-sequencing panel. (a) Evolution of the hexaploid wheat genome. The tetraploid wheat T. turgidum (AABB) originated by the hybridization of T. urartu with the close unidentified relative of Ae. speltoides occurred about 0.58 to 0.82 million years ago according to the genome-wide divergence time estimate [10]. The origin of hexaploid wheat occurred about 10,000 years ago [11] by the hybridization of T. turgidum with Ae. tauschii (DD) [12]. Marcussen et al. [10] suggested that Ae. tauschii might have originated by homoploid hybrid speciation (shown by dashed arrows). (b) Geographic distribution of 62 accessions of wheat accessions. Pie charts indicate the proportion of genetic ancestry for K = 4 inferred using Structure. (c) Efficiency of homoeologous gene capture. The depth of read coverage was extracted for each of the three copies of 47,739 homoeologous gene sets. The histogram of the log2 transformed ratio of read coverage between A and B (red), A and D (blue), and B and D (green) genomes was plotted. Each plot shows a normal distribution with the overall mean at 0. (d) Overlap between the SNP and indel datasets generated by WEC and GBS. (e) Minor allele frequency of different functional classes of SNPs as a proportion of total SNPs within each genome and class. PTC: premature termination codons; SSD: splice-site disruptions.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Summary of re-sequencing panel. (a) Evolution of the hexaploid wheat genome. The tetraploid wheat T. turgidum (AABB) originated by the hybridization of T. urartu with the close unidentified relative of Ae. speltoides occurred about 0.58 to 0.82 million years ago according to the genome-wide divergence time estimate [10]. The origin of hexaploid wheat occurred about 10,000 years ago [11] by the hybridization of T. turgidum with Ae. tauschii (DD) [12]. Marcussen et al. [10] suggested that Ae. tauschii might have originated by homoploid hybrid speciation (shown by dashed arrows). (b) Geographic distribution of 62 accessions of wheat accessions. Pie charts indicate the proportion of genetic ancestry for K = 4 inferred using Structure. (c) Efficiency of homoeologous gene capture. The depth of read coverage was extracted for each of the three copies of 47,739 homoeologous gene sets. The histogram of the log2 transformed ratio of read coverage between A and B (red), A and D (blue), and B and D (green) genomes was plotted. Each plot shows a normal distribution with the overall mean at 0. (d) Overlap between the SNP and indel datasets generated by WEC and GBS. (e) Minor allele frequency of different functional classes of SNPs as a proportion of total SNPs within each genome and class. PTC: premature termination codons; SSD: splice-site disruptions.
Mentions: Wheat genomic variation is shaped by the interplay of multiple factors including two recent polyploidization events [1-3] (Figure 1a), domestication [4], spread from the sites of origin to new geographic regions, gene flow from the populations of wild and domesticated ancestors [5], and post-domestication selection aimed at developing high-yielding locally adapted varieties. The eco-geographic habitats to which wheat is adapted span diverse environments ranging from low humidity regions in Nigeria, and the northern regions of Russia and Norway to the high-humidity regions of South America and Bangladesh [6]. It has been suggested that this broad adaptability likely results from the genetic diversity captured from the natural populations of its tetraploid ancestors [5,7] combined with a high rate of evolutionary changes in the wheat genome (particularly insertions and deletions), which are tolerated by its polyploid nature [8,9].Figure 1

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
Related in: MedlinePlus