Skip to main content
SpringerLink
Log in

Resistance to powdery mildew in one Spanish barley landrace hardly resembles other previously identified wild barley resistances

  • Original Research
  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Two major quantitative trait loci (QTLs) associated with resistance to powdery mildew (Blumeria graminis f. sp. hordei) were previously identified on chromosome 7H of the Spanish barley line SBCC097. The two QTLs seemed to share the same chromosomal position as the major genes mlt and Mlf, which were formerly described in Hordeum vulgare ssp. spontaneum-derived lines. In the present work, different lines that carry mlt (RS42-6*O), Mlf (RS137-28*E), or a combination of both (SI-4 and SI-6) were compared with SBCC097 to evaluate their relatedness at the phenotypic, cellular, and genetic levels. The resistance of the lines was characterised by inoculating them with a set of 27 isolates of B. graminis, which displayed a wide range of virulence. It was revealed that SBCC097 possessed a distinctive resistance spectrum. Microscopic assessment of the cytological development of the resistance response showed that SBCC097 clearly formed fewer well-established colonies and secondary hyphae than the other lines. This was confirmed by the infection type recorded after visual inspection. Genetic analyses of all five lines, based on markers flanking the QTLs derived from SBCC097, supported the macroscopic and microscopic data and pointed to the presence of a combination of novel genes or alleles in SBCC097, which may be included in the category of “intermediate-acting” genes, governing resistance mainly at the post-penetration stage.

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
Fig. 3

Similar content being viewed by others

References

  • Boyd, L. A., Smith, P. H., Foster, E. M., & Brown, J. K. M. (1995). The effects of allelic variation at the Mla resistance locus in barley on the early development of Erysiphe graminis f. sp. hordei and host responses. The Plant Journal, 7, 959–968.

    Article  CAS  Google Scholar 

  • Caldo, R. A., Nettleton, D., Peng, J., & Wise, R. P. (2006). Stage-specific suppression of basal defence discriminates barley plants containing fast- and delayed-acting Mla powdery mildew resistance alleles. Molecular Plant-Microbe Interactions, 19, 939–947.

    Article  PubMed  CAS  Google Scholar 

  • Clark, T. A., Zeyen, R. J., Carver, T. L. W., Smith, A. G., & Bushnell, W. R. (1995). Epidermal cell cytoplasmic events and response gene transcript accumulation during Erysiphe graminis attack in isogenic barley lines differing at the Ml-o locus. Physiological and Molecular Plant Pathology, 46, 1–16.

    Article  CAS  Google Scholar 

  • Conover, W. J. (1980). Practical Nonparametric Statistics. New York: John Wiley & Sons.

    Google Scholar 

  • Czembor, J. H. (1999). Resistance to powdery mildew in barley landraces from Tunisia. Plant Breeding Seed Science, 43, 49–65.

    Google Scholar 

  • Czembor, J. H. (2001). Resistance to powdery mildew in selections from barley landraces collected in Greece. Agricultural and Food Science in Finland, 10, 133–142.

    CAS  Google Scholar 

  • Darken, M. J. (1962). Absorption and transport of fluorescent brighteners by microorganisms. Applied Microbiology, 10, 387–393.

    PubMed  CAS  Google Scholar 

  • Develey-Riviere, M. P., & Galiana, E. (2007). Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytologist, 175, 405–416.

    Article  PubMed  Google Scholar 

  • Dreiseitl, A. (2007). Powdery mildew resistance in winter barley cultivars. Plant Breeding, 126, 268–273.

    Article  CAS  Google Scholar 

  • Eichmann, R., & Hückelhoven, R. (2008). Accomodation of powdery mildew fungi in intact plant cells. Journal of Plant Physiology, 165, 5–18.

    Article  PubMed  CAS  Google Scholar 

  • Faostat (2007). Statistics division of the Food and Agriculture Organization of the United Nations. http://faostat.fao.org. Accessed 15 April 2012.

  • Fischbeck, G., & Jahoor, A. (1991). The transfer of genes for mildew resistance from Hordeum spontaneum. In J. H. Jørgensen (Ed.), Integrated control of cereal mildews: virulence patterns and their change (pp. 247–255). Denmark: Roskilde.

    Google Scholar 

  • Freialdenhoven, A., Scherag, B., Hollricher, K., Collinge, D. B., Thordal-Christensen, H., & Schulze-Lefert, P. (1994). Nar-1 and Nar-2, two loci required for Mla12-specified race-specific resistance to powdery mildew in barley. The Plant Cell, 6, 983–994.

    PubMed  CAS  Google Scholar 

  • Friedt, W., & Ordon, F. (2007). Molecular markers for gene pyramiding and disease resistance breeding in barley. In R. V. Varshney & R. Tuberosa (Eds.), Genomics-assisted crop improvement (Genomics application in crops, Vol. 2, pp. 81–101). Netherlands: Springer.

    Chapter  Google Scholar 

  • Huckelhoven, R., Fodor, J., Trujillo, M., & Kogel, K. H. (2000). Barley Mla and Rar mutants compromised in the hypersensitive cell death response against Blumeria graminis f.sp. hordei are modified in their ability to accumulate reactive oxygen intermediates at sites of fungal invasion. Planta, 212, 16–24.

    Article  PubMed  CAS  Google Scholar 

  • Igartua, E., Gracia, M. P., Lasa, J. M., Medina, B., Molina-Cano, J. L., Montoya, J. L., et al. (1998). The Spanish barley core collection. Genetic Resources and Crop Evolution, 45, 475–481.

    Article  Google Scholar 

  • Jahoor, A. (1986). Mehltauresistenz Israelischer Wildgersten—Resistenzspektrum, Vererbung und Lokalisierung. Dissertation, Technische Universität München, Freising-Weihenstephan.

  • Jahoor, A., & Fischbeck, G. (1987). Genetical studies of resistance of powdery mildew in barley lines derived from Hordeum spontaneum collected from Israel. Plant Breeding, 99, 265–273.

    Article  Google Scholar 

  • Jensen, H. P., Christensen, E., & Jørgensen, J. H. (1992). Powdery mildew resistance genes in 127 Northwest European spring barley varieties. Plant Breeding, 108, 210–228.

    Article  Google Scholar 

  • Jørgensen, J. H., & Jensen, H. P. (1997). Powdery mildew resistance in barley landrace material. I. Screening for resistance. Euphytica, 97, 227–233.

    Article  Google Scholar 

  • Koga, H., Bushnell, W. R., & Zeyen, R. J. (1990). Specificity of cell type and timing of events associated with papilla formation and the hypersensitive reaction in leaves of Hordeum vulgare attacked by Erysiphe graminis f.sp. hordei. Canadian Journal of Botany, 68, 2344–2352.

    Google Scholar 

  • Kruger, W. M., Carver, T. L. W., & Zeyen, R. J. (2002). Phenolic inhibition of penetration resistance to Blumeria graminis f.sp. hordei in barley near isogenic lines containing seven independent resistance genes or alleles. Physiological and Molecular Plant Pathology, 61, 41–51.

    CAS  Google Scholar 

  • Kruger, W. M., Szabo, L. J., & Zeyen, R. J. (2003). Transcription of the defense response genes chitinase IIb, PAL and peroxidase is induced by the barley powdery mildew fungus and is only indirectly modulated by R genes. Physiological and Molecular Plant Pathology, 63, 167–178.

    Article  CAS  Google Scholar 

  • Panstruga, R., Molina-Cano, J. L., Reinstadler, A., & Müller, J. (2005). Molecular characterization of mlo mutants in North American two- and six-rowed malting barley cultivars. Molecular Plant Pathology, 6, 315–320.

    Article  PubMed  CAS  Google Scholar 

  • Prats, E., Gay, A. P., Roberts, P. C., et al. (2010). Blumeria graminis interactions with barley conditioned by different single R genes demonstrate a temporal and spatial relationship between stomatal dysfunction and cell death. Phytopathology, 100, 21–32.

    Article  PubMed  Google Scholar 

  • Proels, R. K., Oberhollenzer, K., Pathuri, I. P., Hensel, G., Kumlehn, J., & Hückelhoven, R. (2010). RBOHF2 of barley is required for normal development of basal penetration resistance to the parasitic fungus Blumeria graminis f. sp. hordei. Molecular Plant-Microbe Interactions, 23, 1143–1150.

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Martín, J., Rubiales, D., & Prats, E. (2011). Resistance to powdery mildew (Blumeria graminis f.sp. avenae) in oat seedlings and adult plants. Plant Pathology, 60, 846–856.

    Article  Google Scholar 

  • Schönfeld, M., Ragni, A., Fischbeck, G., & Jahoor, A. (1996). RFLP mapping of three new loci for resistance genes to powdery mildew (Erysiphe graminis f. sp. hordei) in barley. Theoretical and Applied Genetics, 93, 48–56.

    Article  Google Scholar 

  • Shen, Q. H., Zhou, F., Bieri, S., Haizel, T., Shirasu, K., & Schulze-Lefert, P. (2003). Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus. The Plant Cell, 15, 732–744.

    Article  PubMed  CAS  Google Scholar 

  • Silvar, C., Casas, A. M., Kopahnke, D., Habekuß, A., Schweizer, G., et al. (2010). Screening the Spanish Barley Core Collection for disease resistance. Plant Breeding, 129, 45–52.

    Article  Google Scholar 

  • Silvar, C., Dhif, H., Igartua, E., Kopahnke, D., Gracia, M. P., Lasa, J. M., et al. (2010). Identification of quantitative trait loci for resistance to powdery mildew in a Spanish barley landrace. Molecular Breeding, 25, 581–592.

    Article  CAS  Google Scholar 

  • Silvar, C., Flath, K., Kopahnke, D., Gracia, M. P., Lasa, J. M., Casas, A. M., et al. (2011). Analysis of powdery mildew resistance in the Spanish barley core collection. Plant Breeding, 130, 195–202.

    Article  Google Scholar 

  • Silvar, C., Casas, A. M., Igartua, E., Ponce-Molina, L. J., Gracia, M. P., Schweizer, G., et al. (2011). Resistance to powdery mildew in Spanish barley landraces is controlled by different sets of quantitative trait loci. Theoretical and Applied Genetics, 123, 1019–1028.

    Article  PubMed  CAS  Google Scholar 

  • Silvar, C., Perovic, D., Scholz, U., Casas, A. M., 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. Theoretical and Applied Genetics, 124, 49–62.

    Article  PubMed  Google Scholar 

  • Sugai, K., Masaoka, H., Penjore, K., Hanboonsong, Y., Nishiguchi, M., & Yamaoka, N. (2010). The time and spatial strategy of Blumeria graminis f. sp. hordei for surviving after failure of first infection. Physiological and Molecular Plant Pathology, 74, 346–350.

    Article  Google Scholar 

  • Thordal-Christensen, H., Zhang, Z., Wei, Y., & Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal, 11, 1187–1194.

    Article  CAS  Google Scholar 

  • Yahiaoui, S., Igartua, E., Moralejo, M., Ramsay, L., Molina-Cano, J. L., Ciudad, F. J., et al. (2008). Patterns of genetic and eco-geographical diversity in Spanish barleys. Theoretical and Applied Genetics, 116, 271–282.

    Article  PubMed  CAS  Google Scholar 

  • Zeyen, R. J., Carver, T. L. W., & Lyngkjaer, M. F. (2002). Epidermal cell papillae. In R. R. Belanger, W. R. Bushnell, A. J. Dik, & T. L. W. Carver (Eds.), Powdery mildews: A comprehensive treatise (pp. 107–125). USA: APS Press.

    Google Scholar 

  • Zhang, Z., Henderson, C., Perfect, E., Carver, T. L. W., Thomas, B. J., Skamnioti, P., et al. (2005). Of genes and genomes, needles and haystacks: Blumeria graminis and functionality. Molecular Plant Pathology, 6, 561–575.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the Department of Cellular Biology at the University of Coruña (Spain) for the provision of access to microscopic equipment and to Dr. J.M. Mirás-Avalos for support with the statistical analysis. C.S. held a mobility fellowship from the University of Coruña. Part of the results were obtained within the project ExpResBar funded by the German Federal Ministry of Education and Research under grant number 0315702B within the KBBE-II call, and by the Spanish Ministry of Science and Innovation, grant number EUI2009-04075. Substantial comments from one anonymous reviewer were highly appreciated.

Author information

Authors and Affiliations

  1. Department of Animal and Plant Physiology and Ecology, University of Coruña, 15071, A Coruña, Spain

    Cristina Silvar

  2. Institute for Resistance Research and Stress Tolerance, Julius Kühn Institute, 06484, Quedlinburg, Germany

    Cristina Silvar, Doris Kopahnke, Albrecht Serfling, Dragan Perovic & Frank Ordon

  3. Institute for Plant Protection in Field Crops and Grassland, Julius Kühn Institute, 14532, Kleinmachnow, Germany

    Kerstin Flath

  4. Department of Genetics and Plant Production, Aula Dei Experimental Station, CSIC, 50059, Zaragoza, Spain

    Ana M. Casas & Ernesto Igartua

Authors
  1. Cristina Silvar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doris Kopahnke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kerstin Flath
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Albrecht Serfling
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dragan Perovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ana M. Casas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ernesto Igartua
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Frank Ordon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cristina Silvar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Silvar, C., Kopahnke, D., Flath, K. et al. Resistance to powdery mildew in one Spanish barley landrace hardly resembles other previously identified wild barley resistances. Eur J Plant Pathol 136, 459–468 (2013). https://doi.org/10.1007/s10658-013-0178-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-013-0178-7

Keywords

Search

Navigation