Skip to main content
Log in

Gene-based high-density mapping of the gene rym7 conferring resistance to Barley mild mosaic virus (BaMMV)

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Barley yellow mosaic virus (BaYMV) disease seriously affects winter barley (Hordeum vulgare L.) production. Improvement of resistance to this disease can prevent yield losses. Based on previous reports, the gene rym7 (rmm7), conferring partial resistance to BaMMV, was assigned to chromosome 1H, closely linked to the centromere. In this study, newly developed barley genomic resources were applied to saturate the genetic map at the rym7 locus. Out of a set of 350 gene-based markers of chromosome 1H, we genetically assigned 23 to the rym7 region, delimiting the resistance locus to a 9.9-cM interval close to the centromere by genetic mapping in 53 doubled haploid progeny of a bi-parental mapping population. Nine gene-derived co-dominant markers co-segregated with the resistance locus. Among these, we identified the eukaryotic translation initiation factor Hv-eIF(iso)4E. Its homolog in Arabidopsis thaliana confers resistance to potyviruses. However, sequencing the entire open reading frame of resistant and susceptible genotypes could not reveal any sequence variation in exons of the gene. These results demonstrate how to combine newly developed barley genomic resources for rapid gene-based marker saturation. As a result, several easy-to-handle co-dominant markers have been identified for marker-assisted selection of rym7 in barley breeding.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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(1):133–141

    Article  Google Scholar 

  • Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31(1):24–26

    PubMed  CAS  Google Scholar 

  • Chen JP, Adams MJ, Zhu FT, Wang ZQ, Chen J, Huang SZ, Zhang ZC (1996) Response of foreign barley cultivars to barley yellow mosaic virus at different sites in China. Plant Pathol 45(6):1117–1125

    Article  Google Scholar 

  • Chen J, Shi NN, Cheng Y, Diao A, Chen JP, Wilson TMA, Antoniw JF, Adams MJJ (1999) Molecular analysis of barley yellow mosaic virus isolates from China. Virus Res 64(1):13–21

    Article  PubMed  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(3):475–483

    Article  PubMed  CAS  Google Scholar 

  • Comadran J, Kilian B, Russell J, Ramsay L, Stein N, Ganal M, Shaw P, Bayer M, Thomas W, Marshall D, Hedley P, Tondelli A, Pecchioni N, Francia E, Korzun V, Walther A, Waugh R (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44(12):1388–1392

    Article  PubMed  CAS  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 

  • Duprat A, Caranta C, Revers F, Menand B, Browning KS, Robaglia C (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32(6):927–934

    Article  PubMed  CAS  Google Scholar 

  • Graner A, Streng S, Kellermann A, Proeseler G, Schiemann A, Peterka H, Ordon F (1999a) Molecular mapping of genes conferring resistance to soil-borne viruses in barley—an approach to promote understanding of host-pathogen interactions. Z Pflanzenk Pflanzen 106(4):405–410

    CAS  Google Scholar 

  • Graner A, Streng S, Kellermann A, Schiemann A, Bauer E, Waugh R, Pellio B, Ordon F (1999b) 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(2):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(1):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(9):921–928

    Article  CAS  Google Scholar 

  • Huth W (1989) Ein Jahrzehnt Barley yellow mosaic virus in der Bundesrepublik Deutschland. Nachrichtenbl Dtsch Pflanzenschutzdienst 40:49–55

    Google Scholar 

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

    Google Scholar 

  • IBSC (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716

    Google Scholar 

  • International Brachypodium I (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463(7282):763–768

    Article  Google Scholar 

  • Jenner CE, Nellist CF, Barker GC, Walsh JA (2010) Turnip mosaic virus (TuMV) is able to use alleles of both eIF4E and eIF(iso)4E from multiple loci of the diploid Brassica rapa. Mol Plant Microbe Interact 23(11):1498–1505

    Article  PubMed  CAS  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(3):577–583

    Google Scholar 

  • Kang BC, Yeam I, Jahn MM (2005) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621

    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(5):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(8):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(4):449–458

    Article  PubMed  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Kühne T (2009) Soil-borne viruses affecting cereals—known for long but still a threat. Virus Res 141(2):174–183

    Article  PubMed  Google Scholar 

  • Kühne T, Shi N, Proeseler G, Adams MJ, Kanyuka K (2003) The ability of a bymovirus to overcome the rym4-mediated resistance in barley correlates with a codon change in the VPg coding region on RNA1. J Gen Virol 84(Pt 10):2853–2859

    Article  PubMed  Google Scholar 

  • Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during Potyvirus infection. Curr Biol 12(12):1046–1051

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto T, Tanaka T, Sakai H, Amano N, Kanamori H, Kurita K, Kikuta A, Kamiya K, Yamamoto M, Ikawa H, Fujii N, Hori K, Itoh T, Sato K (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol 156(1):20–28

    Article  PubMed  CAS  Google Scholar 

  • Mayer KF, Martis M, Hedley PE, Simkova H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubalakova M, Suchankova 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, Dolezel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23(4):1249–1263

    Article  PubMed  CAS  Google Scholar 

  • Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18(12):613–615

    Article  PubMed  CAS  Google Scholar 

  • Nishigawa H, Hagiwara T, Yumoto M, Sotome T, Kato T, Natsuaki T (2008) Molecular phylogenetic analysis of Barley yellow mosaic virus. Arch Virol 153(9):1783–1786

    Article  PubMed  CAS  Google Scholar 

  • Nomura K, Kashiwazaki S, Hibino H, Inoue T, Nakata E, Tsuzaki Y, Okuyama S (1996) Biological and serological properties of strains of Barley mild mosaic virus. J Phytopathol 144(2):103–107

    Article  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(1–2):21–28

    Article  CAS  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(2):283–293

    Article  PubMed  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(3):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(1):40–45

    Article  PubMed  CAS  Google Scholar 

  • Ruffel S, Gallois JL, Moury B, Robaglia C, Palloix A, Caranta C (2006) Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. J Gen Virol 87(Pt 7):2089–2098

    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(2):110–117

    Article  PubMed  CAS  Google Scholar 

  • Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jorgensen J-E, Weigel D, Andersen SU (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Meth 6:550–551

    Article  CAS  Google Scholar 

  • Shahinnia F, Druka A, Frankowiak J, Morgante M, 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(2):373–384

    Article  PubMed  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(6):912–922

    Article  PubMed  CAS  Google Scholar 

  • Stein N, Prasad M, Scholz U, Thiel T, Zhang HN, Wolf M, Kota R, Varshney RK, Perovic D, Grosse I, Graner A (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114(5):823–839

    Article  PubMed  CAS  Google Scholar 

  • 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(1):e5

    Article  PubMed  Google Scholar 

  • Van Ooijen TW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherlands

  • Varshney RK, Marcel TC, Ramsay L, Russell J, Roder 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(6):1091–1103

    Article  PubMed  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78

    Article  PubMed  CAS  Google Scholar 

  • Werner K, Friedt W, Ordon F (2005) Strategies for pyramiding resistance genes against the barley yellow mosaic virus complex (BaMMV, BaYMV, BaYMV-2). Mol Breed 16(1):45–55

    Article  CAS  Google Scholar 

  • Zheng T, Cheng Y, Chen JP, Antoniw JF, Adams MJ (1999) The occurrence of Barley mild mosaic virus (BaMMV) in China and the nucleotide sequence of its coat protein gene. J Phytopathol 147(4):229–234

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nils Stein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, P., Perovic, D., Habekuß, A. et al. Gene-based high-density mapping of the gene rym7 conferring resistance to Barley mild mosaic virus (BaMMV). Mol Breeding 32, 27–37 (2013). https://doi.org/10.1007/s11032-013-9842-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-013-9842-z

Keywords

Navigation