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The evolutionary patterns of barley pericentromeric chromosome regions, as shaped by linkage disequilibrium and domestication - PubMed

. 2022 Sep;111(6):1580-1594.

doi: 10.1111/tpj.15908. Epub 2022 Aug 9.

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The evolutionary patterns of barley pericentromeric chromosome regions, as shaped by linkage disequilibrium and domestication

Yun-Yu Chen et al. Plant J. 2022 Sep.

Abstract

The distribution of recombination events along large cereal chromosomes is uneven and is generally restricted to gene-rich telomeric ends. To understand how the lack of recombination affects diversity in the large pericentromeric regions, we analysed deep exome capture data from a final panel of 815 Hordeum vulgare (barley) cultivars, landraces and wild barleys, sampled from across their eco-geographical ranges. We defined and compared variant data across the pericentromeric and non-pericentromeric regions, observing a clear partitioning of diversity both within and between chromosomes and germplasm groups. Dramatically reduced diversity was found in the pericentromeres of both cultivars and landraces when compared with wild barley. We observed a mixture of completely and partially differentiated single-nucleotide polymorphisms (SNPs) between domesticated and wild gene pools, suggesting that domesticated gene pools were derived from multiple wild ancestors. Patterns of genome-wide linkage disequilibrium, haplotype block size and number, and variant frequency within blocks showed clear contrasts among individual chromosomes and between cultivars and wild barleys. Although most cultivar chromosomes shared a single major pericentromeric haplotype, chromosome 7H clearly differentiated the two-row and six-row types associated with different geographical origins. Within the pericentromeric regions we identified 22 387 non-synonymous SNPs, 92 of which were fixed for alternative alleles in cultivar versus wild accessions. Surprisingly, only 29 SNPs found exclusively in the cultivars were predicted to be 'highly deleterious'. Overall, our data reveal an unconventional pericentromeric genetic landscape among distinct barley gene pools, with different evolutionary processes driving domestication and diversification.

Keywords: Hordeum vulgare; SNPs; diversity; domestication; evolution; pericentromeric regions.

© 2022 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

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Conflict of interest statement

The authors declare that they have no conflicts of interest associated with this work.

Figures

Figure 1
Figure 1

Population structure of 815 barley accessions. (a) Principle coordinate analysis (PCO) based on 9845 randomly selected single‐nucleotide polymorphisms (SNPs). Samples are colour coded based on domestication status and row type. The proportion of variance explained by the PCOs are labelled beside the axes. The figure was produced with

curlywhirly

(

https://ics.hutton.ac.uk/curlywhirly/

). (b) Genetic admixture proportion inferred from

faststructure

based on the same 9845 SNPs for the PCO analysis. Colour blocks represent different estimated ancestral populations (K = 7). Samples were grouped based on domestication status and row type, as indicated at the black bars below. The figure was produced using

structure plot

(Ramasamy et al., 2014).

Figure 2
Figure 2

Extensive genetic differentiation in the pericentromeric regions among Hordeum vulgare (barley) groups, showing all single‐nucleotide polymorphisms (SNPs) without minor allele frequency (MAF) filtering. The top track shows the chromosome diagrams, with the gradient of blue colours representing zone 1 (light blue), zone 2 (medium blue) and zone 3 (dark blue) regions, and the red bars representing the centromere, using the coordinates reported by Mascher et al. (2017) and physical distance. (a) Genetic diversity (π): red, wild barleys; orange, landraces; blue, cultivars. (b) Fixation index (F ST) between cultivars and wild barleys. (c) F ST between landraces and wild barleys. (d) F ST between cultivars and landraces. In (b) and (c), sites with F ST ≥ 0.8 were coloured red (with no such sites in panel d).

Figure 3
Figure 3

Diagram of how different wild founder haplotypes give rise to horizontal F ST patterns. (a) In the simplest case, single‐nucleotide polymorphisms (SNPs) in cultivars and wild barleys are fixed completely at two different states and a track of F ST = 1 is formed. (b) Horizontal track with a lower F ST value is formed when some wild barleys share the fixed cultivated allele. (c) ‘Overlapping’ horizontal tracks of F ST formed when different wild barley alleles have varying degrees of differentiation from the cultivars. (d) ‘Break point’ variable horizontal tracks of F ST formed that represent rare recombination between two wild barley founder haplotypes. (e) Real exome sequence genotype data from a segment of barley chromosome 4H, zone 3, showing at least three wild barley founder haplotypes, separated by white space, in this region: the ancestors of the cultivars and one possible double crossover event between different wild founders (asterisk).

Figure 4
Figure 4

Gene haplotype analysis for different barley chromosome zones. Haplotypes of 32 222 genes with variants covered by exome sequencing were characterized. (a) Gene haplotype count by chromosome. (b) Gene haplotype count by chromosome zone. (c) Major haplotype frequency by chromosome. (d) Major haplotype frequency by chromosome zone. (e) Block size (bp) by chromosome. (f) Block size (bp) by chromosome zone. Key: blue, cultivars; orange, landraces; red, wild barleys.

Figure 5
Figure 5

Signatures of positive selection in barley differentiated by chromosome and zone. (a) Selective sweep signal (μ) of barley genomes. Red colours represent genomic regions with μ values above the 95th percentile. The top track shows the chromosome diagrams, with the gradient of blue colours representing zone 1 (light blue), zone 2 (medium blue) and zone 3 (dark blue) regions, and the red bars representing the centromere, using the coordinates reported by Mascher et al. (2017). (b) Distribution of μ values by chromosome for different barley groups. (c) μ values by zone (data from all seven chromosomes combined) for different barley groups.

Figure 6
Figure 6

Maximum‐likelihood (ML) trees for barley constructed using single‐nucleotide polymorphisms (SNPs) from zones 1 and 2, compared with ML tree constructed using zone‐3 SNPs. (a) Chromosome 4H. (b) Chromosome 7H.

Figure 7
Figure 7

Pericentromeric genetic diversity in Hordeum vulgare (barley) visualized as haplogroups. Horizontal lines connecting through each chromosome represent barley accessions (colour coded by domestication status and row type). The vertical position of the line at any given chromosome represents the haplogroup number identified for that accession, based on the order presented in Table S5. The four panels show the diversity profile of: (a) all 815 accessions; (b) cultivars; (c) landraces; and (d) wild barleys.

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