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Genomics-based high-resolution mapping of the BaMMV/BaYMV resistance gene rym11 in barley (Hordeum vulgare L.)

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Abstract

Soil-borne barley yellow mosaic virus disease, caused by different strains of Barley yellow mosaic virus (BaYMV) and Barley mild mosaic virus (BaMMV), is one of the most important diseases of winter barley (Hordeum vulgare L.) in Europe and East Asia. The recessive resistance gene rym11 located in the centromeric region of chromosome 4HL is effective against all so far known strains of BaMMV and BaYMV in Germany. In order to isolate this gene, a high-resolution mapping population (10,204 meiotic events) has been constructed. F2 plants were screened with co-dominant flanking markers and segmental recombinant inbred lines (RILs) were tested for resistance to BaMMV under growth chamber and field conditions. Tightly linked markers were developed by exploiting (1) publicly available barley EST sequences, (2) employing barley synteny to rice, Brachypodium distachyon and sorghum and (3) using next-generation sequencing data of barley. Using this approach, the genetic interval was efficiently narrowed down from the initial 10.72 % recombination to 0.074 % recombination. A marker co-segregating with rym11 was developed providing the basis for gene isolation and efficient marker-assisted selection.

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References

  • Andersen JR, Lübberstedt T (2003) Functional markers in plants. Trends Plant Sci 8:554–560

    Article  PubMed  CAS  Google Scholar 

  • Bauer E, Weyen J, Schiemann A, Graner A, Ordon F (1997) Molecular mapping of novel resistance genes against barley mild mosaic virus (BMMV). Theor Appl Genet 95:1263–1269

    Article  CAS  Google Scholar 

  • Bevan M, Waugh R (2007) Meeting report: applying plant genomics to crop improvement. Genome Biol 8:302

    Article  PubMed  Google Scholar 

  • Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34:475–483

    Article  PubMed  CAS  Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N et al (2009) Development and implementation of high-throughput SNP genoyping in barley. BMC Genomics 10:582

    Article  PubMed  Google Scholar 

  • Comadran J, Ramsay L, MacKenzie K, Hayes P, Close TJ, Muehlbauer G, Stein N, Waugh R (2010) Patterns of polymorphism and linkage disequilibrium in cultivated barley. Theor Appl Genet 122:523–531

    Article  PubMed  Google Scholar 

  • Dorokhov DB, Klocke E (1997) A rapid and economic technique for RAPD analysis of plant genomes. Russ J Gen 33:358–365

    CAS  Google Scholar 

  • Duran C, Appleby N, Vardy M, Imelfort M, Edwardsand D, Batley J (2009) Single nucleotide polymorphism discovery in barley using autoSNPdb. Plant Biotechnol J 7:326–333

    Article  PubMed  CAS  Google Scholar 

  • Dvorák J, Luo MC, Yang ZL (1998) Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing aegilops species. Genetics 148:423–434

    PubMed  Google Scholar 

  • Fraser RSS (1990) The genetics of resistance to plant viruses. Annu Rev Phytopathol 28:179–200

    Article  Google Scholar 

  • Friedt W, Ordon F (2007) Molecular markers for gene pyramiding and disease resistance breeding in barley. In: Varshney R, Tuberosa R (eds) Genomics assisted crop improvement. Springer, Berlin, pp 81–101

    Chapter  Google Scholar 

  • Friedt W, Humbroich K, Ordon F (2008) Genetic diversity of resistance against barley yellow mosaic virus complex in barley. In: Proceedings of the 10th International barley genetics symposium, Alexandria, Egypt, vol 6, pp 7–12

  • Gottwald S, Stein N, Börner A, Sasaki T, Graner A (2004) The gibberellic-acid insensitive dwarfing gene sdw3 of barley is located on chromosome 2HS in a region that shows high colinearity with rice chromosome 7L. Mol Genet Genomics 271:426–436

    Article  PubMed  CAS  Google Scholar 

  • Götz R, Friedt W (1993) Resistance to the barley yellow mosaic virus complex—differential genotypic reactions and genetics of BaMMV-resistance of barley (Hordeum vulgare L.). Plant Breeding 111:125–131

    Article  Google Scholar 

  • Graner A, Streng S, Kellermann A, Schiemann A, Bauer E, Waugh R, Pellio B, Ordon F (1999) Molecular mapping and fine structure of the rym5 locus encoding resistance to different strains of the Barley Yellow Mosaic Virus Complex. Theor Appl Genet 98:285–290

    Article  CAS  Google Scholar 

  • Habekuss A, Kühne T, Krämer I, Rabenstein F, Ehrig F, Ruge-Wehling B, Huth W, Ordon F (2008) Identification of barley mild mosaic virus isolates in Germany breaking rym5 resistance. J Phytopathol 156:36–41

    CAS  Google Scholar 

  • Hanemann A, Schweizer GF, Cossu R, Wicker T, Röder MS (2009) Fine mapping, physical mapping and development of diagnostic markers for the Rrs2 scald resistance gene in barley. Theor Appl Genet 119:1507–1522

    Article  PubMed  CAS  Google Scholar 

  • Hariri D, Meyer M, Le Gouis J, Bahrman N, Fouchard M, Forget C, Andre A (2000) Characterisation of BaYMV and BaMMV pathotypes in France. Eur J Plant Pathol 106:365–372

    Article  CAS  Google Scholar 

  • Hariri D, Meyer M, Prud’homme H (2003) Characterization of a new barley mild mosaic virus pathotype in France. Eur J Plant Pathol 109:921–928

    Article  CAS  Google Scholar 

  • He P, Li JZ, Zheng XW, Shen LS, Lu CF, Chen Y, Zhu LH (2001) Comparison of molecular linkage maps and agronomic trait loci between DH and RIL populations derived from the same rice cross. Crop Sci 41:1240–1246

    Article  CAS  Google Scholar 

  • Hearnden PR, Eckermann PJ, McMichael GL, Hayden MJ, Eglinton JK, Chalmers KJ (2007) A genetic map of 1,000 SSR and DArT markers in a wide barley cross. Theor Appl Genet 115:383–391

    Article  PubMed  CAS  Google Scholar 

  • Hofinger BJ, Russell JR, Bass CG, Baldwin T, Dos Reis M, Hedley PE, Li Y, Macaulay M, Waugh R, Hammond-Kosack KE, Kanyuka K (2011) 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. Mol Ecol. doi:10.1111/j.1365-294X.2011.05201.x

    PubMed  Google Scholar 

  • Huth W (1991) Verbreitung der Gelbmosaikvirosen BaYMV, BaMMV, und BaYMV-2 und Screening von Gerstensorten auf Resistenz gegenüber BaYMV-2. Nachrichtenbl Deut Pflanzenschutzd 43:233–237

    Google Scholar 

  • Kai H, Takata K, Tsukazaki M, Furusho M, Baba T (2012) Molecular mapping of Rym17, a dominant and rym18 a recessive barley yellow mosaic virus (BaYMV) resistance genes derived from Hordeum vulgare L. Theor Appl Genet 124:577–583

    Article  PubMed  CAS  Google Scholar 

  • Kanyuka K, Ward E, Adams MJ (2003) Polymyxa graminis and the cereal viruses it transmits: a research challenge. Mol Plant Pathol 4:393–406

    Article  PubMed  CAS  Google Scholar 

  • Kanyuka K, McGrann G, Alhudaib K, Hariri D, Adams MJ (2004) Biological and sequence analysis of a novel European isolate of Barley mild mosaic virus that overcomes the barley rym5 resistance gene. Arch Virol 149:1469–1480

    Article  PubMed  CAS  Google Scholar 

  • Kanyuka K, Druka A, Caldwell DG, Tymon A, McCallum N, Waugh R, Adams MJ (2005) Evidence that the recessive bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Mol Plant Pathol 6:449–458

    Article  PubMed  CAS  Google Scholar 

  • Kota R, Varshney RK, Prasad M, Zhang H, Stein N, Graner A (2008) EST-derived single nucleotide polymorphism markers for assembling genetic and physical maps of the barley genome. Funct Integr Genomics 8:223–233

    Article  PubMed  CAS  Google Scholar 

  • Kühne T (2009) Soil-borne viruses affecting cereals: known for long but still a threat. Virus Res 141:174–183

    Article  PubMed  Google Scholar 

  • Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412

    PubMed  Google Scholar 

  • Langridge P (2005) Molecular breeding of wheat and barley. In: Tuberosa R, Phillips RL, Gale M (eds) In the wake of the double helix: from the green revolution to the gene revolution. Avenue media, Bologna, pp 279–286

    Google Scholar 

  • Lebel EG, Masson J, Bogucki A, Paszkowski J (1993) Stress-induced intrachromosomal recombination in plant somatic cells. Proc Natl Acad Sci USA 90:422–426

    Article  PubMed  CAS  Google Scholar 

  • López-Moya JJ, Garcia JA (2008) Potyviruses. In: Mahy BWJ, van Regenmortel M (eds) Encyclopedia of virology, 3rd edn. Elsevier, Oxford, pp 313–322

    Chapter  Google Scholar 

  • Maule AJ, Caranta C, Boulton MI (2007) Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8:223–231

    Article  PubMed  CAS  Google Scholar 

  • Mayer KFX, Martis M, Hedley PE, Kimková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Doleqel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263

    Article  PubMed  CAS  Google Scholar 

  • Nissan-Azzouz F, Graner A, Friedt W, Ordon F (2005) Fine-mapping of the BaMMV, BaYMV-1 and BaYMV-2 resistance of barley (Hordeum vulgare) accession PI1963. Theor Appl Genet 110:212–218

    Article  PubMed  CAS  Google Scholar 

  • Ordon F, Götz R, Friedt W (1993) Genetic stocks resistant to barley yellow mosaic viruses (BaMMV, BaYMV, BaYMV-2) in Germany. Barley Genet Newsl 22:46–49

    Google Scholar 

  • Ordon F, Friedt W, Scheurer K, Pellio B, Werner K, Neuhaus G, Huth W, Habekuss A, Graner A (2004) Molecular markers in breeding for virus resistance in barley. J Appl Genet 45:145–159

    PubMed  Google Scholar 

  • Palloix A, Ordon F (2011) Advanced breeding for virus resistance in plants. In: Caranta C, Aranda MA, Tepfer M, Lopez-Moya JJ (eds) Recent advances in plant virology. Caister Academic Press, UK, pp 195–218

    Google Scholar 

  • Pecinka A, Rosa M, Schikora A, Berlinger M, Hirt H, Luschnig C, Mittelsten Scheid O (2009) Transgenerational stress memory is not a general response in Arabidopsis. PLoS One 4:5202

    Article  Google Scholar 

  • Pellio B, Streng S, Bauer E, Stein N, Perovic D, Schiemann A, Friedt W, Ordon F, Graner A (2005) High-resolution mapping of the Rym4/Rym5 locus conferring resistance to the barley yellow mosaic virus complex (BaMMV, BaYMV, BaYMV-2) in barley (Hordeum vulgare ssp. vulgare L.). Theor Appl Genet 110:283–293

    Article  PubMed  CAS  Google Scholar 

  • Perovic D, Stein N, Zhang H, Drescher A, Prasad M, Kota R, Kopahnke D, Graner A (2004) An integrated approach for comparative mapping in rice and barley with special reference to the Rph16 resistance locus. Funct Integr Genomics 4:74–83

    Article  PubMed  CAS  Google Scholar 

  • Perovic D, Tiffin P, Douchkov D, Bäumlein H, Graner A (2007) An integrated approach for the comparative analysis of a multigene family: the nicotianamine synthase genes of barley. Funct Integr Genomics 7:169–179

    Article  PubMed  CAS  Google Scholar 

  • Perovic D, Zorić D, Milovanović M, Prodanović S, Yan Y, Janković S, Šurlan-Momirović G (2009) Hordein gene dose effects in triploid endosperm of barley (Hordeum vulgare L.). Genetika 41:271–287

    Article  Google Scholar 

  • Petes TD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2:360–369

    Article  PubMed  CAS  Google Scholar 

  • Provvidenti R, Hampton RO (1992) Sources of resistance to viruses in the Potyviridae. Arch Virol Suppl 5:189–211

    Article  PubMed  CAS  Google Scholar 

  • Ramsay L, Macaulay M, degli Ivanissevich S, MacLean K, Cardle L, Fuller J, Edwards KJ, Tuvesson S, Morgante M, Massari A, Maestri E, Marmiroli N, Sjakste T, Ganal M, Powell W, Waugh R (2000) A simple sequence repeat-based linkage map of barley. Genetics 156:1997–2005

    PubMed  CAS  Google Scholar 

  • Revers F, Le Gall OT, Candresse T, Maule AJ (1999) New advances in understanding the molecular biology of plant/potyvirus interactions. Mol Plant Microbe Interact 12:367–376

    Article  CAS  Google Scholar 

  • Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Ruge B, Linz A, Pickering R, Proeseler G, Greif P, Wehling P (2003) Mapping of Rym14Hb, a gene introgressed from Hordeum bulbosum and conferring resistance to BaMMV and BaYMV in barley. Theor Appl Genet 107:965–971

    Article  PubMed  CAS  Google Scholar 

  • Ruge-Wehling B, Linz A, Habekuß A, Wehling P (2006) Mapping of Rym16 (Hb), the second soil-borne virus-resistance gene introgressed from Hordeum bulbosum. Theor Appl Genet 113:867–873

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Nankaku N, Takeda K (2009) A high-density transcript linkage map of barley derived from a single population. Heredity 103:110–117

    Article  PubMed  CAS  Google Scholar 

  • Shahinnia F, Sayed-Tabatabaei BE, Sato K, Pourkheirandish M, Komatsuda T (2009) Mapping of QTL for intermedium spike on barley chromosome 4H using EST-based markers. Breeding Sci 59:383–390

    Article  CAS  Google Scholar 

  • Shahinnia F, Druka A, Franckowiak J, Morgante M, Robbie Waugh R, Stein N (2012) High resolution mapping of Dense spike-ar (dsp.ar) to the genetic centromere of barley chromosome 7H. Theor Appl Genet 124:373–384

    Article  PubMed  Google Scholar 

  • Silvar C, Perovic D, Casas AM, Igartua E, Ordon F (2011) Development of a cost-effective pyrosequencing approach for SNP genotyping in barley. Plant Breeding 130:394–397

    Article  CAS  Google Scholar 

  • Silvar C, Perovic D, Scholz U, Casas AM, Igartua E, Ordon F (2012) Fine mapping and comparative genomics integration of two quantitative trait loci controlling resistance to powdery mildew in a Spanish barley landrace. Theor Appl Genet 124:49–62

    Article  PubMed  Google Scholar 

  • Smilde WD, Haluskova J, Sasaki T, Graner A (2001) New evidence for the synteny of rice chromosome 1 and barley chromosome 3H from rice expressed sequence tags. Genome 44:361–367

    Article  PubMed  CAS  Google Scholar 

  • Stein N, Graner A (2004) Map based gene isolation in cereal genomes. In: Gupta PK, Varshney RK (eds) Cereal genomics. Kluwer, Dordrecht, pp 331–360

    Google Scholar 

  • Stein N, Herren G, Keller B (2001) A new DNA extraction method for high-throughput marker analysis in a large genome species such as Triticum aestivum. Plant Breed 120:354–356

    Article  CAS  Google Scholar 

  • Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S, Ordon F, Graner A (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42:912–922

    Article  PubMed  CAS  Google Scholar 

  • Stein N, Prasad M, Scholz U, Thiel T, Zhang H, Wolf M, Kota R, Varshney RK, Perovic D, Graner A (2007) A 1000 loci transcript map of the barley Genome—new anchoring points for integrative grass genomics. Theor Appl Genet 114:823–839

    Article  PubMed  CAS  Google Scholar 

  • Thiel T, Graner A, Waugh R, Grosse I, Close TJ, Stein N (2009) Evidence and evolutionary analysis of ancient whole-genome duplication in barley predating the divergence from rice. BMC Evol Biol 9:209

    Article  PubMed  Google Scholar 

  • Thieme R, Rakosy-Tican E, Gavrilenko T, Antonova O, Schubert J, Nachtigall M, Heimbach U, Thieme T (2008) Novel somatic hybrids (Solanum tuberosum L. + Solanum tarnii) and their fertile BC1 progenies express extreme resistance to potato virus Y and late blight. Theor Appl Genet 116:691–700

    Article  PubMed  CAS  Google Scholar 

  • Timpe U, Kühne T (1994) The complete nucleotide sequence of RNA2 of barley mild mosaic virus (BaMMV). Eur J Plant Pathol 100:233–241

    Article  CAS  Google Scholar 

  • Varshney RK, Marcel TC, Ramsay L, Russell J, Röder MS, Stein N, Waugh R, Langridge P, Niks RE, Graner A (2007) A high density barley microsatellite consensus map with 775 SSR loci. Theor Appl Genet 114:1091–1103

    Article  PubMed  CAS  Google Scholar 

  • Vu GTH, Wicker T, Buchmann JP, Chandler PM, Matsumoto T, Graner A, Stein N (2010) Fine mapping and syntenic integration of the semi-dwarfing gene sdw3 of barley. Funct Integr Genomics 10:509–521

    Article  PubMed  CAS  Google Scholar 

  • Wang ML, Barkley NA, Jenkins TM (2009) Microsatellite markers in plants and insects. Part I: applications of biotechnology. Genes Genomes Genomics 3:54–67

    Google Scholar 

  • Werner K, Friedt W, Laubach E, Waugh R, Ordon F (2003) Dissection of resistance to soil-borne yellow-mosaic-inducing viruses of barley (BaMMV, BaYMV, BaYMV-2) in a complex breeders’ cross by means of SSRs and simultaneous mapping of BaYMV/BaYMV-2 resistance of var. ‘Chikurin Ibaraki 1’. Theor Appl Genet 106:1425–1432

    PubMed  CAS  Google Scholar 

  • Wu Y, Close TJ, Lonardi S (2008) On the accurate construction of consensus genetic maps. Comput Syst Bioinformatics Conf 7:285–296

    PubMed  Google Scholar 

  • Yeam I, Cavatorta JR, Ripoll DR, Kang BC, Jahn MM (2007) Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19:2913–2928

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Karin Ernst and Dörte Grau (JKI) for excellent technical assistance and Susanne König (IPK) for sequencing service. Furthermore, we thank the Federal Ministry of Education and Research (BMBF) for funding this project (FKZ 0314000D) within the BARLEX project.

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Authors and Affiliations

  1. Julius Kuehn-Institute (JKI), Federal Research Centre for Cultivated Plants, Institute for Resistance Research and Stress Tolerance, Erwin-Baur-Str. 27, 06484, Quedlinburg, Germany

    Thomas Lüpken, Dragan Perovic, Antje Habekuß, Ilona Krämer & Frank Ordon

  2. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstr. 3, 06466, Gatersleben, Germany

    Nils Stein, Urs Hähnel, Burkhard Steuernagel, Uwe Scholz, Rounan Zhou & Ruvini Ariyadasa

  3. Leibniz Institute for Age Research, Fritz-Lipmann-Institute (FLI), Beutenbergstraße 11, 07745, Jena, Germany

    Stefan Taudien & Matthias Platzer

  4. Munich Information Center for Protein Sequences/Institute of Bioinformatics and Systems Biology (MIPS/IBIS), Institute for Bioinformatics and Systems Biology, Helmholtz Center Munich, 85764, Neuherberg, Germany

    Mihaela Martis & Klaus Mayer

  5. Institute of Crop Science and Plant Breeding I, Justus-Liebig-University, Heinrich-Buff-Ring 26-32, 35392, Giessen, Germany

    Wolfgang Friedt

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  1. Thomas Lüpken
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Correspondence to Frank Ordon.

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Communicated by P. Hayes.

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Lüpken, T., Stein, N., Perovic, D. et al. Genomics-based high-resolution mapping of the BaMMV/BaYMV resistance gene rym11 in barley (Hordeum vulgare L.). Theor Appl Genet 126, 1201–1212 (2013). https://doi.org/10.1007/s00122-013-2047-3

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