An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations

Bernhard J. Hofinger, Joanne R. Russell, Chris G. Bass, Thomas Baldwin, Mario Dos Reis, Peter E. Hedley, Yidan Li, Malcolm MacAulay, Robbie Waugh, Kim E. Hammond-Kosack, Kostya Kanyuka

    Research output: Contribution to journalArticle

    27 Citations (Scopus)

    Abstract

    In barley, the eukaryotic translation initiation factor 4E (eIF4E) gene situated on chromosome 3H is recognized as an important source of resistance to the bymoviruses Barley yellow mosaic virus and Barley mild mosaic virus. In modern barley cultivars, two recessive eIF4E alleles, rym4 and rym5, confer different isolate-specific resistances. In this study, the sequence of eIF4E was analysed in 1090 barley landraces and noncurrent cultivars originating from 84 countries. An exceptionally high nucleotide diversity was evident in the coding sequence of eIF4E but not in either the adjacent MCT-1 gene or the sequence-related eIF(iso)4E gene situated on chromosome 1H. Surprisingly, all nucleotide polymorphisms detected in the coding sequence of eIF4E resulted in amino acid changes. A total of 47 eIF4E haplotypes were identified, and phylogenetic analysis using maximum likelihood provided evidence of strong positive selection acting on this barley gene. The majority of eIF4E haplotypes were found to be specific to distinct geographic regions. Furthermore, the eI4FE haplotype diversity (uh) was found to be considerably higher in East Asia, whereas SNP genotyping identified a comparatively low degree of genome-wide genetic diversity in 16 of 17 tested accessions (each carrying a different eIF4E haplotype) from this same region. In addition, selection statistic calculations using coalescent simulations showed evidence of non-neutral variation for eIF4E in several geographic regions, including East Asia, the region with a long history of the bymovirus-induced yellow mosaic disease. Together these findings suggest that eIF4E may play a role in barley adaptation to local habitats.

    Original languageEnglish
    Pages (from-to)3653-3668
    Number of pages16
    JournalMolecular Ecology
    Volume20
    Issue number17
    DOIs
    Publication statusPublished - 24 Aug 2011

    Fingerprint

    Eukaryotic Initiation Factor-4E
    Eukaryotic Initiation Factors
    Hordeum
    barley
    Haplotypes
    translation (genetics)
    haplotypes
    allele
    Nucleotides
    nucleotides
    Alleles
    alleles
    phylogenetics
    gene
    phylogeny
    Population
    Genes
    genes
    Mosaic Viruses
    chromosome

    Keywords

    • eIF4E
    • Hordeum vulgare
    • positive selection
    • resistance to viruses
    • single nucleotide polymorphism

    Cite this

    Hofinger, Bernhard J. ; Russell, Joanne R. ; Bass, Chris G. ; Baldwin, Thomas ; Dos Reis, Mario ; Hedley, Peter E. ; Li, Yidan ; MacAulay, Malcolm ; Waugh, Robbie ; Hammond-Kosack, Kim E. ; Kanyuka, Kostya. / An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. In: Molecular Ecology. 2011 ; Vol. 20, No. 17. pp. 3653-3668.
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    abstract = "In barley, the eukaryotic translation initiation factor 4E (eIF4E) gene situated on chromosome 3H is recognized as an important source of resistance to the bymoviruses Barley yellow mosaic virus and Barley mild mosaic virus. In modern barley cultivars, two recessive eIF4E alleles, rym4 and rym5, confer different isolate-specific resistances. In this study, the sequence of eIF4E was analysed in 1090 barley landraces and noncurrent cultivars originating from 84 countries. An exceptionally high nucleotide diversity was evident in the coding sequence of eIF4E but not in either the adjacent MCT-1 gene or the sequence-related eIF(iso)4E gene situated on chromosome 1H. Surprisingly, all nucleotide polymorphisms detected in the coding sequence of eIF4E resulted in amino acid changes. A total of 47 eIF4E haplotypes were identified, and phylogenetic analysis using maximum likelihood provided evidence of strong positive selection acting on this barley gene. The majority of eIF4E haplotypes were found to be specific to distinct geographic regions. Furthermore, the eI4FE haplotype diversity (uh) was found to be considerably higher in East Asia, whereas SNP genotyping identified a comparatively low degree of genome-wide genetic diversity in 16 of 17 tested accessions (each carrying a different eIF4E haplotype) from this same region. In addition, selection statistic calculations using coalescent simulations showed evidence of non-neutral variation for eIF4E in several geographic regions, including East Asia, the region with a long history of the bymovirus-induced yellow mosaic disease. Together these findings suggest that eIF4E may play a role in barley adaptation to local habitats.",
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    author = "Hofinger, {Bernhard J.} and Russell, {Joanne R.} and Bass, {Chris G.} and Thomas Baldwin and {Dos Reis}, Mario and Hedley, {Peter E.} and Yidan Li and Malcolm MacAulay and Robbie Waugh and Hammond-Kosack, {Kim E.} and Kostya Kanyuka",
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    An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. / Hofinger, Bernhard J.; Russell, Joanne R.; Bass, Chris G.; Baldwin, Thomas; Dos Reis, Mario; Hedley, Peter E.; Li, Yidan; MacAulay, Malcolm; Waugh, Robbie; Hammond-Kosack, Kim E.; Kanyuka, Kostya.

    In: Molecular Ecology, Vol. 20, No. 17, 24.08.2011, p. 3653-3668.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations

    AU - Hofinger, Bernhard J.

    AU - Russell, Joanne R.

    AU - Bass, Chris G.

    AU - Baldwin, Thomas

    AU - Dos Reis, Mario

    AU - Hedley, Peter E.

    AU - Li, Yidan

    AU - MacAulay, Malcolm

    AU - Waugh, Robbie

    AU - Hammond-Kosack, Kim E.

    AU - Kanyuka, Kostya

    PY - 2011/8/24

    Y1 - 2011/8/24

    N2 - In barley, the eukaryotic translation initiation factor 4E (eIF4E) gene situated on chromosome 3H is recognized as an important source of resistance to the bymoviruses Barley yellow mosaic virus and Barley mild mosaic virus. In modern barley cultivars, two recessive eIF4E alleles, rym4 and rym5, confer different isolate-specific resistances. In this study, the sequence of eIF4E was analysed in 1090 barley landraces and noncurrent cultivars originating from 84 countries. An exceptionally high nucleotide diversity was evident in the coding sequence of eIF4E but not in either the adjacent MCT-1 gene or the sequence-related eIF(iso)4E gene situated on chromosome 1H. Surprisingly, all nucleotide polymorphisms detected in the coding sequence of eIF4E resulted in amino acid changes. A total of 47 eIF4E haplotypes were identified, and phylogenetic analysis using maximum likelihood provided evidence of strong positive selection acting on this barley gene. The majority of eIF4E haplotypes were found to be specific to distinct geographic regions. Furthermore, the eI4FE haplotype diversity (uh) was found to be considerably higher in East Asia, whereas SNP genotyping identified a comparatively low degree of genome-wide genetic diversity in 16 of 17 tested accessions (each carrying a different eIF4E haplotype) from this same region. In addition, selection statistic calculations using coalescent simulations showed evidence of non-neutral variation for eIF4E in several geographic regions, including East Asia, the region with a long history of the bymovirus-induced yellow mosaic disease. Together these findings suggest that eIF4E may play a role in barley adaptation to local habitats.

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    KW - Hordeum vulgare

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    KW - resistance to viruses

    KW - single nucleotide polymorphism

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