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

Yun Yu Chen; Miriam Schreiber; Micha M. Bayer; Ian K. Dawson; Peter E. Hedley; Li Lei; Alina Akhunova; Chaochih Liu; Kevin P. Smith; Justin C. Fay; Gary J. Muehlbauer; Brian J. Steffenson; Peter L. Morrell; Robbie Waugh; Joanne R. Russell

doi:10.1111/tpj.15908

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

Yun Yu Chen, Miriam Schreiber, Micha M. Bayer, Ian K. Dawson, Peter E. Hedley, Li Lei, Alina Akhunova, Chaochih Liu, Kevin P. Smith, Justin C. Fay, Gary J. Muehlbauer, Brian J. Steffenson, Peter L. Morrell, Robbie Waugh, Joanne R. Russell

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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.

Original language	English (US)
Pages (from-to)	1580-1594
Number of pages	15
Journal	Plant Journal
Volume	111
Issue number	6
DOIs	https://doi.org/10.1111/tpj.15908
State	Published - Sep 2022

Bibliographical note

Funding Information:
This article was a collaborative study and was funded from the following granting bodies: ERC project 669182 ‘SHUFFLE’ (to YYC, MS and RW); European Union's Seventh Framework Programme (FP7/2007–2013) under grant agreement no. FP7‐613556, WHEALBI (to JRR and IKD); Scottish Government Rural and Environment Science and Analytical Services (RESAS) (to JRR, RW, MMB and PEH); USDA‐NIFA Triticeae Coordinated Agricultural Project 2011‐68002‐30029 (to GM, LL, AA, CL and BJS), and National Science Foundation (grant IOS‐1339393) and the Minnesota Agricultural Experiment Station Variety Development fund (to KPS, JCF and PLM). The authors would like to thank Professor Nils Stein and colleagues at Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben. The authors acknowledge the Research/Scientific Computing teams at The James Hutton Institute and the National Institute of Agricultural Botany (NIAB) for providing computational resources and technical support for the ‘UK's Crop Diversity Bioinformatics HPC’ (BBSRC grant BB/S019669/1), the use of which has contributed to the results reported within this paper.

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

Keywords

Hordeum vulgare
SNPs
diversity
domestication
evolution
pericentromeric regions

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Chen, Y. Y., Schreiber, M., Bayer, M. M., Dawson, I. K., Hedley, P. E., Lei, L., Akhunova, A., Liu, C., Smith, K. P., Fay, J. C., Muehlbauer, G. J., Steffenson, B. J., Morrell, P. L., Waugh, R., & Russell, J. R. (2022). The evolutionary patterns of barley pericentromeric chromosome regions, as shaped by linkage disequilibrium and domestication. Plant Journal, 111(6), 1580-1594. https://doi.org/10.1111/tpj.15908

Chen, YY, Schreiber, M, Bayer, MM, Dawson, IK, Hedley, PE, Lei, L, Akhunova, A, Liu, C, Smith, KP, Fay, JC, Muehlbauer, GJ , Steffenson, BJ , Morrell, PL, Waugh, R & Russell, JR 2022, 'The evolutionary patterns of barley pericentromeric chromosome regions, as shaped by linkage disequilibrium and domestication', Plant Journal, vol. 111, no. 6, pp. 1580-1594. https://doi.org/10.1111/tpj.15908

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

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 {\textquoteleft}highly deleterious{\textquoteright}. 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",

author = "Chen, {Yun Yu} and Miriam Schreiber and Bayer, {Micha M.} and Dawson, {Ian K.} and Hedley, {Peter E.} and Li Lei and Alina Akhunova and Chaochih Liu and Smith, {Kevin P.} and Fay, {Justin C.} and Muehlbauer, {Gary J.} and Steffenson, {Brian J.} and Morrell, {Peter L.} and Robbie Waugh and Russell, {Joanne R.}",

note = "Funding Information: This article was a collaborative study and was funded from the following granting bodies: ERC project 669182 {\textquoteleft}SHUFFLE{\textquoteright} (to YYC, MS and RW); European Union's Seventh Framework Programme (FP7/2007–2013) under grant agreement no. FP7‐613556, WHEALBI (to JRR and IKD); Scottish Government Rural and Environment Science and Analytical Services (RESAS) (to JRR, RW, MMB and PEH); USDA‐NIFA Triticeae Coordinated Agricultural Project 2011‐68002‐30029 (to GM, LL, AA, CL and BJS), and National Science Foundation (grant IOS‐1339393) and the Minnesota Agricultural Experiment Station Variety Development fund (to KPS, JCF and PLM). The authors would like to thank Professor Nils Stein and colleagues at Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben. The authors acknowledge the Research/Scientific Computing teams at The James Hutton Institute and the National Institute of Agricultural Botany (NIAB) for providing computational resources and technical support for the {\textquoteleft}UK's Crop Diversity Bioinformatics HPC{\textquoteright} (BBSRC grant BB/S019669/1), the use of which has contributed to the results reported within this paper. Publisher Copyright: {\textcopyright} 2022 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.",

year = "2022",

month = sep,

doi = "10.1111/tpj.15908",

language = "English (US)",

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T1 - The evolutionary patterns of barley pericentromeric chromosome regions, as shaped by linkage disequilibrium and domestication

AU - Chen, Yun Yu

AU - Schreiber, Miriam

AU - Bayer, Micha M.

AU - Dawson, Ian K.

AU - Hedley, Peter E.

AU - Lei, Li

AU - Akhunova, Alina

AU - Liu, Chaochih

AU - Smith, Kevin P.

AU - Fay, Justin C.

AU - Muehlbauer, Gary J.

AU - Steffenson, Brian J.

AU - Morrell, Peter L.

AU - Waugh, Robbie

AU - Russell, Joanne R.

N1 - Funding Information: This article was a collaborative study and was funded from the following granting bodies: ERC project 669182 ‘SHUFFLE’ (to YYC, MS and RW); European Union's Seventh Framework Programme (FP7/2007–2013) under grant agreement no. FP7‐613556, WHEALBI (to JRR and IKD); Scottish Government Rural and Environment Science and Analytical Services (RESAS) (to JRR, RW, MMB and PEH); USDA‐NIFA Triticeae Coordinated Agricultural Project 2011‐68002‐30029 (to GM, LL, AA, CL and BJS), and National Science Foundation (grant IOS‐1339393) and the Minnesota Agricultural Experiment Station Variety Development fund (to KPS, JCF and PLM). The authors would like to thank Professor Nils Stein and colleagues at Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben. The authors acknowledge the Research/Scientific Computing teams at The James Hutton Institute and the National Institute of Agricultural Botany (NIAB) for providing computational resources and technical support for the ‘UK's Crop Diversity Bioinformatics HPC’ (BBSRC grant BB/S019669/1), the use of which has contributed to the results reported within this paper. Publisher Copyright: © 2022 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

PY - 2022/9

Y1 - 2022/9

N2 - 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.

AB - 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.

KW - Hordeum vulgare

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KW - diversity

KW - domestication

KW - evolution

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

Abstract

Bibliographical note

Keywords

UN SDGs

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