Theoretical and Applied Genetics

, Volume 126, Issue 12, pp 2969–2982 | Cite as

Fine mapping and chromosome walking towards the Ror1 locus in barley (Hordeum vulgare L.)

  • Johanna Acevedo-Garcia
  • Nicholas C. Collins
  • Nahal Ahmadinejad
  • Lu Ma
  • Andreas Houben
  • Pawel Bednarek
  • Mariam Benjdia
  • Andreas Freialdenhoven
  • Janine Altmüller
  • Peter Nürnberg
  • Richard Reinhardt
  • Paul Schulze-Lefert
  • Ralph PanstrugaEmail author
Original Paper


Key message

The Ror1 gene was fine-mapped to the pericentric region of barley chromosome 1HL.


Recessively inherited loss-of-function alleles of the barley (Hordeum vulgare) Mildew resistance locus o (Mlo) gene confer durable broad-spectrum disease resistance against the obligate biotrophic fungal powdery mildew pathogen Blumeria graminis f.sp. hordei. Previous genetic analyses revealed two barley genes, Ror1 and Ror2, that are Required for mlo-specified resistance and basal defence. While Ror2 was cloned and shown to encode a t-SNARE protein (syntaxin), the molecular nature or Ror1 remained elusive. Ror1 was previously mapped to the centromeric region of the long arm of barley chromosome 1H. Here, we narrowed the barley Ror1 interval to 0.18 cM and initiated a chromosome walk using barley yeast artificial chromosome (YAC) clones, next-generation DNA sequencing and fluorescence in situ hybridization. Two non-overlapping YAC contigs containing Ror1 flanking genes were identified. Despite a high degree of synteny observed between barley and the sequenced genomes of the grasses rice (Oryza sativa), Brachypodium distachyon and Sorghum bicolor across the wider chromosomal area, the genes in the YAC contigs showed extensive interspecific rearrangements in orientation and order. Consequently, the position of a Ror1 homolog in these species could not be precisely predicted, nor was a barley gene co-segregating with Ror1 identified. These factors have prevented the molecular identification of the Ror1 gene for the time being.


Powdery Mildew Yeast Artificial Chromosome Barley Chromosome Barley Gene Yeast Artificial Chromosome Clone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



R.P, J.A.G and M.B were funded by grants from the Max Planck Society. J.A.G was additionally supported by a research fellowship from the International Max Planck Research School (IMPRS). N.C.C gratefully acknowledges Syngenta for funding. Work in the P.B lab is supported by an EMBO Installation Grant. We are thankful to Margaret Corbitt for technical assistance, Takuji Sasaki and Robin Buell for sharing rice genomics information pre-publication, Pietro Spanu for performing pulsed field gel electrophoresis of YACs and Akio Kato for providing the probe pHv1112.

Supplementary material

122_2013_2186_MOESM1_ESM.pdf (68 kb)
Supplementary material 1 (PDF 68 kb) File S1 Non-coding sequences derived from de novo assembly of YAC sequence reads
122_2013_2186_MOESM2_ESM.png (1.5 mb)
Supplementary material 2 (PNG 1536 kb) Fig. S1 Micrographs of multicolor FISH on barley metaphase chromosomes of cv. Ingrid. Shown in white (in merged) is the signal of the chromosome 1H long arm-specific probe pHv-1112 (Kato 2011); the arrows indicate the position of the signals for the genic probes in green and red; the insets show a magnification of the chromosomes with the FISH signals in black and white and after pseudo-coloring (in part rotated to suit the Figure format, arrow head indicates the pHv-1112-specific signal). Scale bar = 20 µm. a Probes for Con (red) + Pol (green) + pHv-1112. b Con (red) + Unk (green) + pHv-1112. Note that only results for combinations 1 and 2 (see main text) are shown and that the different chromosome background colors in Fig. 3 (blue) and Fig. S1 (greenish) are due to the fact that results shown in Fig. S1 are multicolor overlays of three differently labeled probes, lacking a dedicated color for the chromosomes
122_2013_2186_MOESM3_ESM.png (545 kb)
Supplementary material 3 (PNG 544 kb) Fig. S2 Accumulation of selected secondary metabolites in first leaves of the indicated barley genotypes at 24 and 48 hours after inoculation with Blumeria graminis f. sp. hordei spores. Compounds with retention time (RT) 10.9, 12.3, 14.1 and 16.2 minutes are shown as the ones representing the most striking induction after pathogen inoculation. Error bars indicate standard deviations of one experiment
122_2013_2186_MOESM4_ESM.png (148 kb)
Supplementary material 4 (PNG 148 kb) Fig. S3 UV spectra for four UPLC-PDA metabolite peaks showing induction by Blumeria graminis f. sp. hordei inoculation in primary barley leaves. Representative UV spectra of compounds eluted at retention time (RT) 14.1 and 16.2 resemble those reported for hordatines, their precursors and derivatives (Stoessl and Unwin 1970; von Röpenack et al. 1998). AU, absorbance units
122_2013_2186_MOESM5_ESM.xlsx (15 kb)
Supplementary material 5 (XLSX 15 kb) Table S1 Primer pairs used to amplify the Pol and Con genes and selected YAC ends
122_2013_2186_MOESM6_ESM.xlsx (18 kb)
Supplementary material 6 (XLSX 17 kb) Table S2 Detail of primer pairs used to investigate the genes from the YAC clones and the genomic DNA sequence obtained for each gene fragment in the parents Ingrid and Malteria Heda
122_2013_2186_MOESM7_ESM.xlsx (12 kb)
Supplementary material 7 (XLSX 11 kb) Table S3 Primer pairs used to amplify unique probes for barley FISH
122_2013_2186_MOESM8_ESM.xls (119 kb)
Supplementary material 8 (XLS 119 kb) Table S4 Details of DNA sequence polymorphism survey across three barley mapping parent genotypes
122_2013_2186_MOESM9_ESM.xls (52 kb)
Supplementary material 9 (XLS 52 kb) Table S5 Polymorphisms, haplotypes and marker details for the three barley mapping parent genotypes
122_2013_2186_MOESM10_ESM.xls (50 kb)
Supplementary material 10 (XLS 50 kb) Table S6 Genotypes of F2 recombinants for the Ror1 interval, used for fine mapping
122_2013_2186_MOESM11_ESM.xlsx (14 kb)
Supplementary material 11 (XLSX 13 kb) Table S7 Genotype in a panel of recombinants for the Ror1 interval for the genes identified in the sequenced YAC clones
122_2013_2186_MOESM12_ESM.xlsx (16 kb)
Supplementary material 12 (XLSX 16 kb) Table S8 Anchoring option, position coordinates and contigs in the barley genome for the genes present in the sequenced YAC clones close to the Ror1 locus. The analysis is based on the International Barley Sequencing Consortium (2012) genome draft release and


  1. Altschul S, Gish W, Miller W, Myers E, Lipman D et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P et al (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106PubMedCrossRefGoogle Scholar
  3. Bednarek P, Piślewska-Bednarek M, van Loren Themaat E, Maddula RK, Svatoš A, Schulze-Lefert P et al (2011) Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives. New Phytol 192:713–726PubMedCrossRefGoogle Scholar
  4. Bennetzen JL, Ramakrishna W (2002) Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol Biol 48:821–827PubMedCrossRefGoogle Scholar
  5. Bjørnstad Å, Demissie A, Kilian A, Kleinhofs A et al (1997) The distinctness and diversity of Ethiopian barleys. Theor Appl Genet 94:514–521CrossRefGoogle Scholar
  6. Bowers JE, Arias MA, Asher R, Avise JA, Ball RT, Brewer GA, Buss RW, Chen AH, Edwards TM, Estill JC, Exum HE, Goff VH, Herrick KL, Steele SLM, Karunakaran S, Lafayette GK, Lemke C, Marler BS, Masters SL, McMillan JM, Nelson LK, Newsome GA, Nwakanma CC, Odeh RN, Phelps CA, Rarick EA, Rogers CJ, Ryan SP, Slaughter KA, Soderlund CA, Tang H, Wing RA, Paterson AH et al (2005) Comparative physical mapping links conservation of microsynteny to chromosome structure and recombination in grasses. Proc Natl Acad Sci USA 102:13206–13211PubMedCrossRefGoogle Scholar
  7. Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A et al (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA 99:9328–9333PubMedCrossRefGoogle Scholar
  8. Brunner S, Keller B, Feuillet C (2003) A large rearrangement involving genes and low-copy DNA interrupts the microcollinearity between rice and barley at the Rph7 locus. Genetics 164:673–683PubMedGoogle Scholar
  9. Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P et al (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705PubMedCrossRefGoogle Scholar
  10. Chaplin DD, Brownstein BH (2001a) Analysis of isolated YAC clones. Curr Protoc Mol Biol. doi: 10.1002/0471142727.mb0610s20 (John Wiley & Sons, Inc., pp 6.10.11–16.10.19)Google Scholar
  11. Chaplin DD, Brownstein BH (2001b) Overview of strategies for screening YAC libraries and analyzing YAC clones. Curr Protoc Mol Biol. doi: 10.1002/0471142727.mb0609s20 (John Wiley & Sons, Inc., pp 6.9.1–6.9.7)Google Scholar
  12. Chen A, Brûlé-Babel A, Baumann U, Collins NC (2009) Structure-function analysis of the barley genome: the gene-rich region of chromosome 2HL. Funct Integr Genomics 9:67–79PubMedCrossRefGoogle Scholar
  13. Collins NC, Lahaye T, Peterhänsel C, Freialdenhoven A, Corbitt M, Schulze-Lefert P et al (2001) Sequence haplotypes revealed by sequence-tagged site fine mapping of the Ror1 gene in the centromeric region of barley chromosome 1H. Plant Physiol 125:1236–1247PubMedCrossRefGoogle Scholar
  14. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P et al (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977PubMedCrossRefGoogle Scholar
  15. Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, Schulze-Lefert P, Somerville SC, Panstruga R et al (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38:716–720PubMedCrossRefGoogle Scholar
  16. Consonni C, Bednarek P, Humphry M, Francocci F, Ferrari S, Harzen A, Ver Loren van Themaat E, Panstruga R et al (2010) Tryptophan-derived metabolites are required for antifungal defense in the Arabidopsis mlo2 mutant. Plant Physiol 152:1544–1561PubMedCrossRefGoogle Scholar
  17. Devoto A, Piffanelli P, Nilsson I, Wallin E, Panstruga R, von Heijne G, Schulze-Lefert P et al (1999) Topology, subcellular localization, and sequence diversity of the Mlo family in plants. J Biol Chem 274:34993–35004PubMedCrossRefGoogle Scholar
  18. Draper J, Mur LAJ, Jenkins G, Ghosh-Biswas GC, Bablak P, Hasterok R, Routledge APM et al (2001) Brachypodium distachyon. A new model system for functional genomics in grasses. Plant Physiol 127:1539–1555PubMedCrossRefGoogle Scholar
  19. Favret E (1965) Induced mutations in breeding for disease resistance. In: Nations FaAOotU (ed) The use of induced mutations in plant breeding. Pergamon Press, London, pp 521–536Google Scholar
  20. Foote TN, Griffiths S, Allouis S, Moore G (2004) Construction and analysis of a BAC library in the grass Brachypodium sylvaticum: its use as a tool to bridge the gap between rice and wheat in elucidating gene content. Funct Integr Genomics 4:26–33PubMedCrossRefGoogle Scholar
  21. Freialdenhoven A, Peterhänsel C, Kurth J, Kreuzaler F, Schulze-Lefert P et al (1996) Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8:5–14PubMedGoogle Scholar
  22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  23. Hückelhoven R, Trujillo M, Kogel K-H et al (2000) Mutations in Ror1 and Ror2 genes cause modification of hydrogen peroxide accumulation in mlo-barley under attack from the powdery mildew fungus. Mol Plant Pathol 1:287–292PubMedCrossRefGoogle Scholar
  24. Humphry M, Bednarek P, Kemmerling B, Koh S, Stein M, Göbel U, Stüber K, Piślewska-Bednarek M, Loraine A, Schulze-Lefert P, Somerville S, Panstruga R et al (2010) A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity. Proc Natl Acad Sci USA 107:21896–21901PubMedCrossRefGoogle Scholar
  25. Jarosch B, Kogel K-H, Schaffrath U (1999) The ambivalence of the barley Mlo locus: mutations conferring resistance against powdery mildew (Blumeria graminis f. sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol Plant Microbe Interact 12:508–514CrossRefGoogle Scholar
  26. Jarosch B, Collins NC, Zellerhoff N, Schaffrath U et al (2005) RAR1, ROR1, and the actin cytoskeleton contribute to basal resistance to Magnaporthe grisea in barley. Mol Plant Microbe Interact 18:397–404PubMedCrossRefGoogle Scholar
  27. Jørgensen J (1976) Identification of powdery mildew resistant barley mutants and their allelic relationship. In: Gaul H (ed) Barley genetics III: Proceedings of the third international barley genetics symposium, Verlag Karl Thiemig, Garching, 7–12 July 1975, pp 446–455Google Scholar
  28. Jørgensen JH (1992a) Sources and genetics of resistance to fungal pathogens. In: Shewry PR (ed) Barley: genetics, biochemestry, molecular biology and biotechnology. CAB International, Wallingford, Oxfordshire, UK, pp 441–457Google Scholar
  29. Jørgensen JH (1992b) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63:141–152CrossRefGoogle Scholar
  30. Kalendar R, Lee D, Schulman A (2009) FastPCR software for PCR primer and probe design and repeat search. Genes Genomes Genomics 3:1–14Google Scholar
  31. Kato A (2011) High-density fluorescence in situ hybridization signal detection on barley (Hordeum vulgare L.) chromosomes with improved probe screening and reprobing procedures. Genome 54:151–159PubMedCrossRefGoogle Scholar
  32. Kato A, Albert P, Vega J, Birchler J (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech Histochem 81:71–78PubMedCrossRefGoogle Scholar
  33. Kilian A, Chen J, Han F, Steffenson B, Kleinhofs A (1997) Towards map-based cloning of the barley stem rust resistance genes Rpg1 and rpg4 using rice as an intergenomic cloning vehicle. Plant Mol Biol 35:187–195PubMedCrossRefGoogle Scholar
  34. Kumar J, Hückelhoven R, Beckhove U, Nagarajan S, Kogel K-H et al (2001) A compromised Mlo pathway affects the response of barley to the necrotrophic fungus Bipolaris sorokiniana (teleomorph: Cochliobolus sativus) and its toxins. Phytopathology 91:127–133PubMedCrossRefGoogle Scholar
  35. Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412PubMedGoogle Scholar
  36. Kwaaitaal M, Keinath NF, Pajonk S, Biskup C, Panstruga R et al (2010) Combined Bimolecular Fluorescence Complementation and Förster Resonance Energy Transfer reveals ternary SNARE complex formation in living plant cells. Plant Physiol 152:1135–1147PubMedCrossRefGoogle Scholar
  37. Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, Kasmi FE, Jurgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P et al (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451:835–840PubMedCrossRefGoogle Scholar
  38. Lahaye T, Hartmann S, Töpsch S, Freialdenhoven A, Yano M, Schulze-Lefert P et al (1998) High-resolution genetic and physical mapping of the Rar1 locus in barley. Theor Appl Genet 97:526–534CrossRefGoogle Scholar
  39. Langmead B, Trapnell C, Pop M, Salzberg S et al (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25PubMedCrossRefGoogle Scholar
  40. Li B, Choulet F, Heng YF, Hao WW, Paux E, Liu Z, Yue W, Jin WW, Feuillet C, Zhang XY et al (2013) Wheat centromeric retrotransposons: the new ones take a major role in centromeric structure. Plant J 73:952–965PubMedCrossRefGoogle Scholar
  41. Ma L, Vu G, Schubert V, Watanabe K, Stein N, Houben A, Schubert I et al (2010) Synteny between Brachypodium distachyon and Hordeum vulgare as revealed by FISH. Chromosome Res 18:841–850PubMedCrossRefGoogle Scholar
  42. 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 et al (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol 156:20–28PubMedCrossRefGoogle Scholar
  43. Mayer KFX, Martis M, Hedley PE, Simková 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, Dolezel J, Waugh R, Stein N et al (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263PubMedCrossRefGoogle Scholar
  44. Meyer D, Pajonk S, Micali C, O’Connell R, Schulze-Lefert P et al (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57:986–999PubMedCrossRefGoogle Scholar
  45. Ogilvie DJ, James LA (1996) End rescue from YACs using the vectorette. In: Marki D (ed) YAC Protocols, Methods in molecular biology, vol 54. Humana Press, New York, USA, pp 131–138Google Scholar
  46. Orabi J, Backes G, Wolday A, Yahyaoui A, Jahoor A et al (2007) The horn of Africa as a centre of barley diversification and a potential domestication site. Theor Appl Genet 114:1117–1127PubMedCrossRefGoogle Scholar
  47. Peterhänsel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze-Lefert P et al (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9:1397–1409PubMedGoogle Scholar
  48. Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P et al (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129:1076–1085PubMedCrossRefGoogle Scholar
  49. Pourkheirandish M, Wicker T, Stein N, Fujimura T, Komatsuda T et al (2007) Analysis of the barley chromosome 2 region containing the six-rowed spike gene vrs1 reveals a breakdown of rice–barley micro collinearity by a transposition. Theor Appl Genet 114:1357–1365PubMedCrossRefGoogle Scholar
  50. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP et al (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26PubMedCrossRefGoogle Scholar
  51. Ruiz-Lozano JM, Gianinazzi S, Gianinazzi-Pearson V (1999) Genes involved in resistance to powdery mildew in barley differentially modulate root colonization by the mycorrhizal fungus Glomus mosseae. Mycorrhiza 9:237–240CrossRefGoogle Scholar
  52. Schmidt D, Röder M, Dargatz H, Wolf N, Schweizer G, Tekauz A, Ganal M et al (2001) Construction of a YAC library from barley cultivar Franka and identification of YAC-derived markers linked to the Rh2 gene conferring resistance to scald (Rhynchosporium secalis). Genome 44:1031–1040PubMedGoogle Scholar
  53. Shirasu K, Lahaye T, Tan M-W, Zhou F, Azevedo C, Schulze-Lefert P et al (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99:355–366PubMedCrossRefGoogle Scholar
  54. Shure M, Wessler S, Fedoroff N (1983) Molecular identification and isolation of the Waxy locus in maize. Cell 35:225–233PubMedCrossRefGoogle Scholar
  55. Simons G, van der Lee T, Diergaarde P, van Daelen R, Groenendijk J, Frijters A, Büschges R, Hollricher K, Töpsch S, Schulze-Lefert P, Salamini F, Zabeau M, Vos P et al (1997) AFLP-based fine mapping of the Mlo gene to a 30-kb DNA segment of the barley genome. Genomics 44:61–70PubMedCrossRefGoogle Scholar
  56. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol İ et al (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123PubMedCrossRefGoogle Scholar
  57. Stein N, Prasad M, Scholz U, Thiel T, Zhang H, Wolf M, Kota R, Varshney R, Perovic D, Grosse I, Graner A et al (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114:823–839PubMedCrossRefGoogle Scholar
  58. Stoessl A, Unwin CH (1970) The antifungal factors in barley. V. Antifungal activity of the hordatines. Can J Bot 48:465–470CrossRefGoogle Scholar
  59. Takamatsu S (2004) Phylogeny and evolution of the powdery mildew fungi (Erysiphales, Ascomycota) inferred from nuclear ribosomal DNA sequences. Mycoscience 45:147–157CrossRefGoogle Scholar
  60. Taketa S, You T, Sakurai Y, Miyake S, Ichii M et al (2011) Molecular mapping of the short awn 2 (lks2) and dense spike 1 (dsp1) genes on barley chromosome 7H. Breed Sci 61:80–85CrossRefGoogle Scholar
  61. The International Barley Genome Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716Google Scholar
  62. Trujillo M, Troeger M, Niks RE, Kogel K-H, Hückelhoven R et al (2004) Mechanistic and genetic overlap of barley host and non-host resistance to Blumeria graminis. Mol Plant Pathol 5:389–396PubMedCrossRefGoogle Scholar
  63. von Röpenack E, Parr A, Schulze-Lefert P (1998) Structural analyses and dynamics of soluble and cell wall-bound phenolics in a broad spectrum resistance to the powdery mildew fungus in barley. J Biol Chem 273:9013–9022CrossRefGoogle Scholar
  64. Wicker T, Buchmann JP, Keller B (2010) Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res 20:1229–1237PubMedCrossRefGoogle Scholar
  65. Wicker T, Mayer KFX, Gundlach H, Martis M, Steuernagel B, Scholz U, Šimková H, Kubaláková M, Choulet F, Taudien S, Platzer M, Feuillet C, Fahima T, Budak H, Doležel J, Keller B, Stein N et al (2011) Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives. Plant Cell 23:1706–1718PubMedCrossRefGoogle Scholar
  66. Xu Z, Escamilla-Treviño L, Zeng L, Lalgondar M, Bevan D, Winkel B, Mohamed A, Cheng C-L, Shih M-C, Poulton J, Esen A et al (2004) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Mol Biol 55:343–367PubMedCrossRefGoogle Scholar
  67. Zhang W-J, Pedersen C, Kwaaitaal M, Gregersen PL, Mørch SM, Hanisch S, Kristensen A, Fuglsang AT, Collinge DB, Thordal-Christensen H et al (2012) Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Mol Plant Pathol 13:1110–1119PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Johanna Acevedo-Garcia
    • 1
    • 3
  • Nicholas C. Collins
    • 2
    • 7
  • Nahal Ahmadinejad
    • 1
    • 8
  • Lu Ma
    • 4
  • Andreas Houben
    • 4
  • Pawel Bednarek
    • 10
  • Mariam Benjdia
    • 1
    • 9
  • Andreas Freialdenhoven
    • 6
  • Janine Altmüller
    • 5
  • Peter Nürnberg
    • 5
  • Richard Reinhardt
    • 1
  • Paul Schulze-Lefert
    • 1
  • Ralph Panstruga
    • 1
    • 3
    Email author
  1. 1.Department of Plant-Microbe InteractionsMax Planck Institute for Plant Breeding ResearchCologneGermany
  2. 2.Sainsbury LaboratoryJohn Innes CentreNorwichUK
  3. 3.Unit of Plant Molecular Cell Biology, Institute for Biology IRWTH Aachen UniversityAachenGermany
  4. 4.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK)Stadt SeelandGermany
  5. 5.Cologne Center for Genomics (CCG)University of CologneCologneGermany
  6. 6.Institute for Biology IRWTH Aachen UniversityAachenGermany
  7. 7.Australian Centre for Plant Functional Genomics, School of Agriculture Food and WineUniversity of AdelaideGlen OsmondAustralia
  8. 8.INRES, Crop BioinformaticsUniversity of BonnBonnGermany
  9. 9.European Commission ERC Executive Agency, COV2BrusselsBelgium
  10. 10.Institute of Bioorganic ChemistryPolish Academy of SciencesPoznanPoland

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