Skip to main content

Advertisement

SpringerLink
Log in

Analysis of bymovirus resistance genes on proximal barley chromosome 4HL provides the basis for precision breeding for BaMMV/BaYMV resistance

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Unlocking allelic diversity of the bymovirus resistance gene rym11 located on proximal barley chromosome 4HL and diagnostic markers provides the basis for precision breeding for BaMMV/BaYMV resistance.

Abstract

The recessive resistance gene rym11 on barley chromosome 4HL confers broad-spectrum and complete resistance to all virulent European isolates of Barley mild mosaic virus and Barley yellow mosaic virus (BaMMV/BaYMV). As previously reported, rym11-based resistance is conferred by a series of alleles of naturally occurring deletions in the gene HvPDIL5-1, encoding a protein disulfide isomerase-like protein. Here, a novel resistance-conferring allele of rym11 is reported that, in contrast to previously identified resistance-conferring variants of the gene HvPDIL5-1, carries a single non-synonymous amino acid substitution. Allelism was confirmed by crossing to genotypes carrying previously known rym11 alleles. Crossing rym11 genotypes with a cultivar carrying the recessive resistance gene rym1, which was reported to reside on the same chromosome arm 4HL like rym11, revealed allelism of both loci. This allelic state was confirmed by re-sequencing HvPDIL5-1 in the rym1 genotype, detecting the haplotype of the rym11-d allele. Diagnostic PCR-based markers were established to differentiate all seven resistance-conferring alleles of the rym11 locus providing precise tools for marker-assisted selection (MAS) of rym11 in barley breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adams MJ (1991) The distribution of Barley Yellow Mosaic-Virus (BaYMV) and Barley Mild Mosaic-Virus (BaMMV) in UK winter barley samples, 1987–1990. Plant Pathol 40:53–58

    Article  Google Scholar 

  • Adams MJ, Swaby AG, Jones P (1988) Confirmation of the transmission of Barley Yellow Mosaic Virus (BaYMV) by the fungus Polymyxa graminis. Ann Appl Biol 112:133–141

    Article  Google Scholar 

  • Bauer E, Weyen J, Schiemann A, Graner A, Ordon F (1997) Molecular mapping of novel resistance genes against Barley Mild Mosaic Virus (BaMMV). Theor Appl Genet 95:1263–1269

    Article  CAS  Google Scholar 

  • Charron C, Nicolai M, Gallois JL, Robaglia C, Moury BT, Palloix A, Caranta C (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54:56–68

    Article  CAS  PubMed  Google Scholar 

  • Chen JP (2005) Progress and prospects of studies on Polymyxa graminis and its transmitted cereal viruses in China. Prog Nat Sci 15:481–490

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Goetz 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 Breed 111:125–131

    Article  Google Scholar 

  • Graner A, Bauer E (1993) RFLP mapping of the Ym4 virus-resistance gene in barley. Theor Appl Genet 86:689–693

    Article  CAS  PubMed  Google Scholar 

  • Graner A, Streng S, Kellermann A, Schiemann A, Bauer E, Waugh R, Pellio B, Ordon F (1999) Molecular mapping and genetic 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, Kuhne T, Kramer 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

    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 

  • Humbroich K (2007) Identification and mapping of resistance genes against soil-borne viruses barley (Hordeum vulgare L.) and wheat (Triticum aestivum L.). PhD thesis, in Agricultural and nutritional sciences, Justus-Liebig-University, Halle, Germany, p 96

  • Humbroich K, Jaiser H, Schiemann A, Devaux P, Jacobi A, Cselenyi L, Habekuss A, Friedt W, Ordon F (2010) Mapping of resistance against Barley mild mosaic virus-Teik (BaMMV)—an rym5 resistance breaking strain of BaMMV - in the Taiwanese barley (Hordeum vulgare) cultivar ‘Taihoku A’. Plant Breed 129:346–348

    Article  CAS  Google Scholar 

  • Huth W (1989) Ein weiterer Stamm des Barley yellow mosaic virus gefunden. Nachrichtenbl Dt Pflanzenschutzd 41:6–7

    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  CAS  PubMed  Google Scholar 

  • Kaiser R, Friedt W (1992) Gene for resistance to Barley Mild Mosaic Virus in german winter barley located on Chromosome 3L. Plant Breed 108:169–172

    Article  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Kashiwazaki S, Ogawa K, Usugi T, Omura T, Tsuchizaki T (1989) Characterization of several strains of barley yellow mosaic virus. Ann Phytopathol Soc Jap 55:16–25

    Article  Google Scholar 

  • Konishi T, Kaiser-Alexnat R (2000) Reaction of barley accessions to BaYMV and BaMMV in Japan, compared with data in Germany. Barley Genet Newsl 30:58–62

    Google Scholar 

  • Konishi T, Ban T, Iida Y, Yoshimi R (1997) Genetic analysis of disease resistance to all strains of BaYMV in a Chinese barley landrace, Mokusekko 3. Theor Appl Genet 94:871–877

    Article  Google Scholar 

  • Konishi T, Ordon F, Furusho M (2002) Reactions of barley accessions carrying different rym genes to BaYMV and BaMMV in Japan and Germany. Barley Genet Newsl 32:46–48

    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 

  • Lüpken T, Stein N, Perovic D, Habekuss A, Kramer I, Hahnel U, Steuernagel B, Scholz U, Zhou R, Ariyadasa R, Taudien S, Platzer M, Martis M, Mayer K, Friedt W, Ordon F (2013) Genomics-based high-resolution mapping of the BaMMV/BaYMV resistance gene rym11 in barley (Hordeum vulgare L.). Theor Appl Genet 126:1201–1212

    Article  PubMed  Google Scholar 

  • Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Okada Y, Kashiwazaki S, Kanatani R, Arai S, Ito K (2003) Effects of barley yellow mosaic disease resistant gene rym1 on the infection by strains of Barley yellow mosaic virus and Barley mild mosaic virus. Theor Appl Genet 106:181–189

    CAS  PubMed  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 

  • Ordon F, Ahlemeyer J, Werner K, Kohler W, Friedt W (2005) Molecular assessment of genetic diversity in winter barley and its use in breeding. Euphytica 146:21–28

    Article  CAS  Google Scholar 

  • Plumb RT, Lennon EA, Gutteridge RA (1986) The effects of infection by Barley yellow mosaic virus on the yield and components of yield of barley. Plant Pathol 35:314–318

    Article  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Steyer S, Kummert J, Froidmont F (1995) Characterization of a resistance-breaking BaYMV isolate from Belgium. Agronomie 15:433–438

    Article  Google Scholar 

  • Takahashi R, Hayashi J, Inouye T, Moriya I, Hirao C (1973) Studies on resistance to yellow mosaic disease in barley. I. Tests for varietal reactions and genetic analysis of resistance to the disease. Ber Ohara Inst 16:1–17

  • Thiel T, Kota R, Grosse I, Stein N, Graner A (2004) SNP2CAPS: a SNP and INDEL analysis tool for CAPS marker development. Nucleic Acids Res 32:e5

    Article  PubMed Central  PubMed  Google Scholar 

  • Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74

    Article  PubMed Central  PubMed  Google Scholar 

  • Werner K, Pellio B, Ordon F, Friedt W (2000) Development of an STS marker and SSRs suitable for marker-assisted selection for the BaMMV resistance gene rym9 in barley. Plant Breed 119:517–519

    Article  CAS  Google Scholar 

  • Werner K, Ronicke S, Le Gouis J, Friedt W, Ordon F (2003) Mapping of a new BaMMV-resistance gene derived from the variety ‘Taihoku A’. Z Pflanzenk Pflanzen 110:304–311

    CAS  Google Scholar 

  • Yang P, Perovic D, Habekuss A, Zhou RN, Graner A, Ordon F, Stein N (2013) Gene-based high-density mapping of the gene rym7 conferring resistance to Barley mild mosaic virus (BaMMV). Mol Breed 32:27–37

    Article  Google Scholar 

  • Yang P, Lüpken T, Habekuss A, Hensel G, Steuernagel B, Kilian B, Ariyadasa R, Himmelbach A, Kumlehn J, Scholz U, Ordon F, Stein N (2014) Protein disulfide isomerase like 5-1 is a susceptibility factor to plant viruses. Proc Natl Acad Sci 111:2104–2109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge Jelena Perovic (IPK) and Dörte Grau (JKI) for excellent technical support. The work was financially supported as part of the collaborative project ‘‘Plant KBBE II-ViReCrop’’ by a grant (FKZ 0315708) of the German Ministry of Education and Research (BMBF) to NS and FO.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Genome Diversity, Department Genebank, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstraße 3, 06466, Stadt Seeland (OT) Gatersleben, Germany

    Ping Yang & Nils Stein

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

    Antje Habekuß & Frank Ordon

Authors
  1. Ping Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Antje Habekuß
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frank Ordon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nils Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nils Stein.

Additional information

Communicated by Takao Komatsuda.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, P., Habekuß, A., Ordon, F. et al. Analysis of bymovirus resistance genes on proximal barley chromosome 4HL provides the basis for precision breeding for BaMMV/BaYMV resistance. Theor Appl Genet 127, 1625–1634 (2014). https://doi.org/10.1007/s00122-014-2324-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-014-2324-9

Keywords

Search

Navigation