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The Barley/Blumeria (Syn. Erysiphe) Graminis Interaction

  • Chapter
Mechanisms of Resistance to Plant Diseases

Summary

Barley leaves attacked by the powdery mildew fungus is a pathosystem well suited for studies of plant-pathogen interaction mechanisms. Nearly one hundred specific resistance genes have been identified, many of which are alleles at more or less complex loci. The corresponding avirulence genes are, on the other hand, evenly distributed in the powdery mildew fungus genome. The fungus colonizes only the leaf surface, placing haustoria in the leaf epidermal cells to acquire nutrients in an obligately biotrophic manner. The fungus exhibits a highly synchronous development and the epidermal cells respond accordingly. Papillae, which are formed early, subjacent to fungal germ tubes, arrest a considerable fraction of the attempted penetrations in all combinations of pathogen and plant genotypes (i.e. both incompatible and compatible). Papillae consist of several different components, and inhibitor studies have suggested that at least callose and phenylpropanoids are directly involved in arresting the growth of the penetration peg. In compatible interactions, the haustorial nutrient uptake is believed to be driven by fungal plasma membrane H+-ATPase activity. This is based on the apparent lack of H+-ATPase activity at the invaginated host plasma membrane. In incompatible interactions, the hypersensitive response serves as a back-up resistance mechanism arresting the germlings which have managed to penetrate the papilla. While only limited information is available concerning the expression of pathogenicity genes in the powdery mildew fungus, significantly more is known in relation to host response gene expression. However, the biological role of the host response genes is poorly understood; data suggest that many of them are merely part of a general stress response with no direct involvement in defense.

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Abbreviations

Bhg:

Blumeria graminis f.sp. hordei

CAD:

cinnamyl alcohol dehydrogenase

CHS:

chalcone synthase

OMT:

O-methyltransferase

PAL:

phenylalanine ammonia lyase

PGT:

primary germ tube

PR:

pathogenesis-related

References

  • Aist JR and Bushnell WR (1991) Invasion of plants by powdery mildew fungi, and cellular mechanisms of the resistance. In: Cole GT and Hoch HC (eds) The Fungal Spore and Disease Initiation in Plants and Animals, pp 321–345. Plenum Press, New York

    Google Scholar 

  • Aist JR and Israel HW (1977) Papilla formation: Timing and significance during penetration of barley coleoptiles by Erysiphe graminis hordei. Phytopathol 67: 455–461

    Google Scholar 

  • Aist JR, Gold RE, Bayles CJ, Morrison GH, Chandra S and Israel HW (1988) Evidence that molecular components of papillae may be involved in ml-o resistance to barley powdery mildew. Physiol Mol Plant Pathol 33: 17–32

    CAS  Google Scholar 

  • Akutsu K, Doi Y and Yora K (1980) Elementary analysis of papillae and cytoplasmic vesicles formed at the penetration site by Erysiphe graminis f.sp. hordei in epidermal cells of barley leaves. Ann Phytopathol Soc Japan 46: 667–671

    Google Scholar 

  • Bayles CJ, Ghemawat MS and Aist JR (1990) Inhibition by 2-deoxy-D-glucose of callose formation, papilla deposition, and resistance to powdery mildew in an ml-o barley mutant. Physiol Mol Plant Pathol 36: 63–72

    CAS  Google Scholar 

  • Bohlmann H, Clausen S, Behnke S, Giese H, Hiller C, Reimann-Philipp U, Schrader G, Barkholt V and Apel K (1988) Leaf-specific thionins of barley — a novel class of cell wall proteins toxic to plant-pathogic fingi and possibly involved in the defence mechanism of plants. EMBO J 7: 1559–1565

    PubMed  CAS  Google Scholar 

  • Boyd LA, Smith PH and Brown JKM (1994a) Molecular and cellular expression of quantitative resistance in barley to powdery mildew. Physiol Mol Plant Pathol 45 47–58

    CAS  Google Scholar 

  • Boyd LA, Smith PH, Green RM and Brown JKM (1994b) The relationship between the expression of defense-related genes and mildew development in barley. Mol Plant-Micr Interact 7 401–410

    CAS  Google Scholar 

  • Boyd LA, Smith PH, Foster EM and Brown JKM (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. Plant J 7: 959–968

    CAS  Google Scholar 

  • Bracker CE (1968) Ultrastructure of the haustorial apparatus of Erysiphe graminis and its relationship to the epidermal cell of barley. Phytopathol 58: 12–30.

    Google Scholar 

  • Brandt J, Thordal-Christensen H, Vad K, Gregersen PL and Collinge DB (1992) A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. Plant J 2: 815–820

    PubMed  CAS  Google Scholar 

  • Bryngelsson T, Sommer-Knudsen J, Gregersen PL, Collinge DB, Ek B and Thordal-Christensen H (1994). Purification, characterization, and molecular cloning of basic PR-1-type pathogenesis-related proteins form barley. Mol Plant-Micr Interac 7: 267–275

    CAS  Google Scholar 

  • Bryngelsson T and Gréen B (1989) Characterization of a pathogenesis-related protein, thaumatin-like protein isolated from barley challenged with an incompatible race of mildew. Physiol Mol Plant Pathol 35: 45–52

    CAS  Google Scholar 

  • 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 and Schulze-Lefert P (1997) The barley Mlo gene: A novel control element of plant pathogen resistance. Cell 88: 695–705

    PubMed  Google Scholar 

  • Bushneil WR (1981) Incompatibility conditioned by the Mla gene in powdery mildew of barley: The halt in cytoplasmic streaming. Phytopathol 71: 1062–1066

    Google Scholar 

  • Bushnell WR (1985) Expression of race-specific incompatibility in powdery mildew: implications for mechanisms of gene action. In Sussex I, Ellingboe A, Crouch M and Malmberg R (eds) Plant Cell/Cell Interactions, pp 83–87. Cold Spring Harbor, New York

    Google Scholar 

  • Bushnell WR and Gay J (1978) Accumulation of solutes in relation to the structure and function of haustoria in powdery mildews. In: Spencer DM (ed) The Powdery Mildews, pp 183–235. Academic Press, London

    Google Scholar 

  • Bushnell WR and Liu Z (1994) Incompatibility conditioned by the Mla gene in powdery mildew of barley: timing of the effect of cordycepin on hypersensitive cell death. Physiol Molec Plant Pathol 44: 389–402

    CAS  Google Scholar 

  • Bushnell WR and Zeyen RJ (1976) Light and electron microscope studies of cytoplasmic aggregates formed in barley cells in response to Erysiphe graminis. Can J Bot 54: 1647–1655

    Google Scholar 

  • Carver TLW (1986) Histology of infection by Erysiphe graminis f.sp. hordei in spring barley lines with various levels of partial resistance. Plant Pathol 35: 232–240

    Google Scholar 

  • Carver TLW and Bushnell WR (1983) The probable role of primary germ tubes in water uptake before infection by Erysiphe graminis. Physiol Plant Pathol 23: 229–240

    Google Scholar 

  • Carver TLW and Ingerson SM (1987) Responses of Erysiphe graminis germlings to contact with artificial and host surfaces. Physiol Mol Plant Pathol 30: 359–372

    Google Scholar 

  • Carver TLW and Ingerson-Morris SM (1989) Effects of inoculum density on germling development by Erysiphe graminis f.sp. avenae in relation to induced resistance of oat cells to appressorial penetration. Mycol Res 92: 18–24

    Google Scholar 

  • Carver TLW, Zeyen RJ, Bushnell WR and Robbins MP (1994) Inhibition of Phenylalanine ammonia lyase and cinnamyl alcohol dehrydrogenase increases quantitative susceptibility of barley to powdery mildew (Erysiphe graminis D.C.). Physiol Mol Plant Pathol 44: 261–272

    CAS  Google Scholar 

  • Carver TLW, Zeyen RJ, Robbins MP and Dearne GA (1992) Effects of the PAL inhibitor, AOPP, on oat, barley and wheat cell responses to appropriate and inappropriate formae specials of Erysiphe graminis DC. Physiol Mol Plant Pathol 41: 397–409

    CAS  Google Scholar 

  • Carver TLW, Zhang L, Zeyen RJ and Robbins MP (1996) Phenolic biosynthesis inhibitor suppress adult plant resistance to Erysiphe graminis in oat at 20°C and 10°C. Physiol Mol Plant Pathol 49: 121–141

    CAS  Google Scholar 

  • Christensen AB, Gregersen PL, Olsen CE and Collinge DB (1998a) A flavonoid 7-O-methyltransferase is expressed in barley leaves in response to pathogen attack. Plant Mol Biol 36 219–227

    PubMed  CAS  Google Scholar 

  • Christensen AB, Gregersen PL, Schröder J and Collinge DB (1998b) A chalcone synthase with unusual substrate pReferences is expressed in barley leaves in response to UV light and pathogen attack. Plant Mol Biol 37 849–857

    PubMed  CAS  Google Scholar 

  • Cho BH and Smedegaard-Petersen V (1986) Induction of resistance to Erysiphe graminis f.sp. hordei in near-isogenic barley lines. Phytopathol 76: 301–305

    Google Scholar 

  • Christiansen SK and Giese H (1990) Genetic analysis of the obligate parastic barley powdery mildew fungus based on RFLP and virulence loci. Theor Appl Gen 79: 705–712

    CAS  Google Scholar 

  • Clark TA, Zeyen RJ, Carver TLW, Smith AG and Bushnell WR (1995) Epidermal cell cytoplasmic events and response gene transcript accumulation during Erysiphe graminis attack in isogenic barley lines differing at the Ml-o locus. Physiol Mol Plant Pathol 46: 1–16

    CAS  Google Scholar 

  • Clark TA, Zeyen RJ, Smith AG, Bushnell WR, Szabo LJ and Vance CP (1993) Host response gene transcript accumulation in relation to visible cytological events during Erysiphe graminis attack in isogenic barley lines differing at the Ml-a locus. Physiol Mol Plant Pathol 43: 283–298

    CAS  Google Scholar 

  • Clark TA, Zeyen RJ, Smith AG, Carver TLW and Vance CP (1994) Phenylalanine ammonia lyase mRNA accumulation, enzyme activity and cytoplasmic responses in barley isolines, differing at MI-a and Ml-o loci, attacked by Erysiphe graminis f.sp. hordei. Physiol Mol Plant Pathol 44: 171–185

    CAS  Google Scholar 

  • Collinge DB, Bryngelsson T, Gregersen PL, Smedegaard-Petersen V and Thordal-Christensen H (1997) Resistance against fungal pathogens: its nature and regulation. In: Basra AS and Basra R (eds) Mechanisms of Environmental Stress Resistance in Plants, pp 335–372. Harwood Academic Publishers, Chur, Switzerland

    Google Scholar 

  • Davidson AD, Manners JM, Simpson RS and Scott KJ (1988) Altered host gene expression in near-isogenic barley conditioned by different genes for resistance during infection by Erysiphe graminis f.sp. hordei. Physiol Mol Plant Path 32: 127–139

    CAS  Google Scholar 

  • DeScenzo RA, Wise RP and Mahadevappa M (1994) High-resolution mapping of the Horl/Mla/Hor2 region on chromosome 5S in barley. Mol Plant-Micr Interact 7: 657–666

    CAS  Google Scholar 

  • Dumas B, Freyssinet G and Pallett KE (1995) Tissue-specific expression of germin-like Oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiol 107: 1091–1096

    PubMed  CAS  Google Scholar 

  • Ebrahim-Nesbat F, Bohl S, Heitefuss R and Apel K (1993) Thionin in cell walls and papillae of barley in compatible and incompatible interactions with Erysiphe graminis f.sp. hordei. Physiol Mol Plant Pathol 43: 343–352

    CAS  Google Scholar 

  • Edwards HH and Allen PJ (1970) A fine-structure of the primary infection process during infection of barley by Erysiphe graminis f.sp. hordei. Phytopathol 60: 1504–1509

    Google Scholar 

  • Francis SA, Dewey FM and Gurr SJ (1996) The role of cutinase in germling development and infection by Erysiphe graminis f.sp. hordei. Physiol Mol Plant Pathol 49: 201–211

    CAS  Google Scholar 

  • Freialdenhoven A, Scherag B, Hollricher K, Collinge DB, Thordal-Christensen H and Schulze-Lefert P (1994) Nar-1 and Nar-2, two loci required for Mla 12-specified race-specific resistance to powdery mildew in barley. Plant Cell 6: 983–994

    PubMed  CAS  Google Scholar 

  • Freialdenhoven A, Peterhänsel C, Kurth J, Kreuzaler F and Schulze-Lefert P (1996) Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8: 5–14

    PubMed  CAS  Google Scholar 

  • Gay JL, Salzberg A and Woods AM (1987) Dynamic experimental evidence for the plasma membrane ATPase domain hypothesis of haustorial transport and for ionic coupling of the haustorium of Erysiphe graminis to the host cell (Hordeum vulgare). New Phytol 107: 541–548

    CAS  Google Scholar 

  • Giese H, Holm-Jensen AG, Jensen HP and Jensen J (1993) Localization of the Laevigatum powdery mildew resistance gene to barley chromosome 2 by use of RFLP markers. Theor Appl Genet 85: 897–900

    CAS  Google Scholar 

  • Gregersen PL, Christensen AB, Sommer-Knudsen J and Collinge DB (1994) A putative O-methyltransferase from barley is induced by fungal pathogens and UV light. Plant Mol Biol 26: 1797–1806

    PubMed  CAS  Google Scholar 

  • Gregersen PL, Thordal-Christensen H, Förster H and Collinge DB (1997) Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f.sp. hordei. Physiol Mol Plant Pathol 51: 85–97

    CAS  Google Scholar 

  • Gold RE, Aist JR, Hazen BE, Stolzenburg, Marshall MR and Israel HW (1986) Effect of calcium nitrate and Chlortetracycline on papilla formation, ml-o resistance and susceptibility of barley to powdery mildew. Physiol Mol Plant Pathol 29: 115–129

    CAS  Google Scholar 

  • Görg R, Hollricher K and Schulze-Lefert P (1993) Functional analysis and RFLP mapping of the Mlg resistance gene in barley. Plant J 3: 857–866

    Google Scholar 

  • Hall JL, Aked J, Gregory AJ and Storr T (1992) Carbon metabolism and transport in a biotrophic fungal association. In: Pollock CJ, Farrar JF and Gordon AJ (eds) Carbon Partitioning Within and Between Organisms, pp 181–198. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Heitefuss R and F Ebrahim-Nesbat (1986) Ultrastructural and histochemical studies on mildew of barley (Erysiphe graminis DC. f.sp. hordei Marchai). III. Ultrastructure of different types of papillae in susceptible and adult plant resistant leaves. J Phytopathol 116: 358–373

    Google Scholar 

  • Hippe-Sanwald S, Hermanns M and Somerville SC (1992) Ultrastructural comparison of incompatible and compatible interactions in the barley powdery mildew disease. Protoplasma 168: 27–40

    Google Scholar 

  • Hilbers S, Fischbeck G and Jahoor A (1992) Localization of the lavigatum resistance gene Ml-La against powdery mildew in the barley genome by the use of RFLP markers. Plant Breed 109: 335–338

    CAS  Google Scholar 

  • Hiura U (1978) Genetic basis of formae speciales in Erysiphe graminis. In: Spencer DM (ed) The Powdery Mildews, pp 101–128. Academic Press, London

    Google Scholar 

  • Jahoor A, Jacobi A, Schüller CME and Fischbeck G (1993) Genetical and RFLP studies at the Mla locus conferring powdery mildew resistance in barley. Theor Appl Genet 85: 713–718

    CAS  Google Scholar 

  • Johnson LEB, Bushneil WR and Zeyen RJ (1979) Binary pahways for analysis of primary infection and host response in populations of powdery mildew fungi. Can J Bot 57: 497–511

    Google Scholar 

  • Jørgensen JH (1988) Erysiphe graminis, powdery mildew of cereals and grasses. Adv Plant Pathol 6: 137–157

    Google Scholar 

  • Jørgensen JH (1994) Genetics of powdery mildew resistance in barley. Crit Rev Plant Sci 13: 97–119

    Google Scholar 

  • Jørgensen JH and Mortensen K (1977) Primary infection by Erysiphe graminis f.sp. hordei of barley mutants with resistance genes in the ml-o locus. Phytopathol 67: 678–685

    Google Scholar 

  • Jørgensen JH, Munk L and Kølster P (1988) Svampesygdom i byg koster samfundet millioner hvert år. Forskning og Samfundet 2: 10–12

    Google Scholar 

  • Justesen A, Somerville SC, Christiansen SK and Giese H (1995) Isolation and characterization of two novel genes expressed in germinating conidia of the obligate biotroph Erysiphe graminis f.sp. hordei. Gene 170: 131–135

    Google Scholar 

  • Jutidamrongpham W, Andersen JB, Mackinnon G, Manners JM, Simpson RS and Scott KJ (1991) Induction of β-l,3-glucanase in barley in response to infection by fungal pathogens. Mol Plant-Microb Interact 4: 234–238

    Google Scholar 

  • Kauss H (1992) Callose and callose synthase. In: Gurr SJ, McPherson MJ and Bowles DJ (eds) Molecular Plant Pathology: A Practical Approach, Vol II, pp 1–8. IRL Press, Oxford

    Google Scholar 

  • Kerby K and Somerville S (1989) Enhancement of specific intercellular peroxidases following inoculation of barley with Erysiphe graminis f.sp. hordei. Physiol Mol Plant Pathol 35: 323–337

    CAS  Google Scholar 

  • Kerby K and Somerville SC (1992) Purification of an infection-related, extracellular peroxidase from barley. Plant Physiol 100: 397–402

    PubMed  CAS  Google Scholar 

  • Kita N, Toyoda H and Shishiyama J (1980) Histochemical reactions of papilla and cytoplasmic aggregate in epidermal cells of barley leaves infected by Erysiphe graminis hordei. Ann Phytopathol Soc Japan 46: 263–265

    Google Scholar 

  • Kita N, Toyoda H and Shishiyama J (1981) Chronological analysis of cytological responses in powdery mildewed barley leaves. Can J Bot 59: 1761–1768

    Google Scholar 

  • Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T and Kunoh H (1997) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J 11: 525–537.

    CAS  Google Scholar 

  • Kobayashi I, Watababe H and Kunoh H (1995) Induced accessibility and enhanced inaccessibility at the cellular level in barley coleoptiles. XIV. Evidence for elicitor(s) and suppressor(s) of host inaccessibility from Erysiphe graminis. Physiol Mol Plant Pathol 46: 445–456

    Google Scholar 

  • Koch G and Köhler W (1990) Isozyme variation and genetic distances of Erysiphe graminis DC formae speciales. J Phytopathol 89: 89–101

    Google Scholar 

  • Koch G and Köhler W (1991) Isozyme variation and genetic diversity of the European barley powdery mildew population. J Phytopathol 131: 333–344

    CAS  Google Scholar 

  • Koga H, Bushneil WR and Zeyen RJ (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. Can J Bot 68: 2344–2352

    Google Scholar 

  • Koga H, Zeyen RJ, Bushneil WR and Ahlstrand GG (1988) Hypersensitive cell death, autofluorescence, and insoluble silicon accumulation in barley leaf epidermal cells under attack by Erysiphe graminis f.sp. hordei. Physiol Mol Plant Pathol 32: 395–409

    Google Scholar 

  • Kragh KM, Jacobsen S and Mikkelsen JD (1990) Induction, purification and characterization of barley leaf chitinase. Plant Sci 71: 55–68

    CAS  Google Scholar 

  • Kragh KM, Jacobsen S, Mikkelsen JD and Nielsen KA (1993) Tissue specificity and induction of class I, II and III chitinase in barley (Hordeum vulgare). Physiol Plant 89: 490–498

    CAS  Google Scholar 

  • Kunoh H (1995) Host-parasite specificity in powdery mildews. In: Kohmoto K, Singh US and Singh RP (eds) Pathogenesis and Host Specificity in Plant Diseases: Histopathology, Biochemistry, Genetic and Molecular Bases, Vol II: Eukaryotes, pp 239–250. Elsevier, Oxford

    Google Scholar 

  • Kunoh H, Itoh O, Kohno M and Ishizaki H (1979) Are primary germ tubes of conidia unique to Erysiphe graminis? Ann Phytopathol Soc Japan 45: 675–682

    Google Scholar 

  • Kunoh H and Ishizaki H (1976) Accumulation of chemical elements around the penetration sites of Erysiphe graminis hordei on barley leaf epidermis: (III) micromanipulation and X-ray microanalysis of silicon. Physiol Plant Pathol 8: 91–96

    CAS  Google Scholar 

  • Kunoh H and Ishizaki H (1981) Cytological studies of early stages of powdery mildew in barley and wheat. VII. Reciprocal translocation of a fluorescent dye between barley coleoptile cells and conidia. Physiol Plant Patho 18: 207–211

    Google Scholar 

  • Kunoh H, Kuroda K, Hayashimoto A and Ishizaki H (1986) Induced accessibility and enhanced resistance at the cellular level in barley coleoptiles. II. Timing and localization of induced susceptibility in a single coleoptile cell andits transfer to an adjacent cell. Can J Bot 64: 889–895

    Google Scholar 

  • Kunoh H, Komura T, Yamaoka N and Kobayashi I (1988a) Induced accessibility and enhanced inaccessibility at the cellular level in barley coleoptiles. IV. Escape of the second lobe of the Erysiphe graminis appressorium from inaccessibility enhanced by the previous attack of the first lobe. Ann Phytopath Soc Japan 54 577–583

    Google Scholar 

  • Kunoh H, Nicholson RL, Yoshioka H, Yamaoka N and Kobayashi I (1990) Preparation of the infection court by Erysiphe graminis: Degradation of the host cuticle. Physiol Molec Plant Pathol 36: 397–407.

    CAS  Google Scholar 

  • Kunoh H, Takamatsu S and Ishizaki H (1978a) Cytological studies of early stages of powdery mildew in barley and wheat. III. Distribution of residual calcium and silicon in germinated conidia of Erysiphe graminis hordei. Physiol Plant Pathol 13 319–325

    CAS  Google Scholar 

  • Kunoh H, Tsuzuki T and Ishizaki H (1978b) Cytological studies of early stages of powdery mildew in barley and wheat. IV. Direct ingress from superficial primary germ tubes and appressorial of Erysiphe graminis hordei on leaves of barley. Physiol Plant Pathol 13 327–333

    Google Scholar 

  • Kunoh H, Yamaoka N, Yoshioka H and Nicholson RL (1988b) Preparation of the infection court by Erysiphe graminis I. Contact-mediated changes in morphology of the conidium surface. Exp Mycol 12 352–335.

    Google Scholar 

  • Kølster P, Munk L, Stølen O and Løhde J (1986) Near-isogenic barley lines with genes for resistance to powdery mildew. Crop Sci 26: 903–907

    Google Scholar 

  • Lee-Stadelmann OY, Curran CM and Bushnell WR (1992) Incompatibility conditioned by the Mla gene in powdery mildew of barley: change in permeability to non-electrolytes. Physiol Mol Plant Pathol 41: 165–177

    Google Scholar 

  • Lyngkjær MF, Jensen HP and Østergård H (1995) A Japanese powdery mildew isolate with exceptionally large infection efficiency on Mlo-resistant barley. Plant Pathol 44: 786–790

    Google Scholar 

  • Mahadevappa M, DeScenzo RA and RP Wise (1994) Recombination of alleles conferring specific resistance to powdery mildew at the Mla locus in barley. Genome 37: 460–468

    PubMed  CAS  Google Scholar 

  • Manners JM and Gay JL (1977) The morphology of haustorial complexes isolated from apple, barley, beet and vine infected with powdery mildews. Physiol Plant Pathol 11: 261–266

    Google Scholar 

  • Manners JM and Gay JL (1983) The host-parasite interface and nutrient transfer in biotrophic parasitism. In: Callow JA (ed) Biochemical Plant Pathology, pp 163–195. John Wiley & Sons, Chichester

    Google Scholar 

  • Masri SS and Ellingboe AH (1966) Primary infection of wheat and barley by Erysiphe graminis. Phytopathol 56: 253–378

    Google Scholar 

  • McKeen WE and Rimmer SR (1973) Initial penetration process in powdery mildew infection of susceptible barley leaves. Phytopathol 63: 1049–1053

    Google Scholar 

  • Mehdy MC (1994) Active oxygen species in plant defence against pathogens. Plant Physiol 105: 467–472

    PubMed  CAS  Google Scholar 

  • Mendgen K and Nass P (1988) The activity of powdery-mildew haustoria after feeding the host cells with different sugars, as measured with a Potentiometric cyanine dye. Planta 174: 283–288

    CAS  Google Scholar 

  • Molina A and Garcí-Olmedo F (1993) Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins. Plant J 4: 983–991

    PubMed  CAS  Google Scholar 

  • Mount MS and Ellingboe AH (1969) 32P and 35S transfer from susceptible wheat to Erysiphe graminis f.sp. tritici during primary infection. Phytopathol 59: 235

    Google Scholar 

  • Muradov A, Petrasovits L, Davidson A and Scott KJ (1993) A cDNA clone for a pathogenesis-related protein 1 from barley. Plant Mol Biol 23: 439–442

    PubMed  CAS  Google Scholar 

  • Nicholson RL, Yoshioka H, Yamaoka N and Kunoh H (1988) Preparation of the infection court by Erysiphe graminis II. Release of esterase enzyme from conidia in response to a contact stimulus. Exp Mycol 12: 336–349

    CAS  Google Scholar 

  • Ouchi S, Oku H, Hibino C and Akiyama I (1974) I. Induction of accessibility and enhanced resistance in leaves of barley by some races of Erysiphe graminis. Phytopathol Z 79: 24–34

    Google Scholar 

  • Pascholati SF, Yoshioka H, Kunoh H and Nicholson RL (1992) Preparation of the infection court by Erysiphe graminis f.sp. hordei: cutinase is a component of the conidial exudate. Physiol Molec Plant Pathol 41: 53–59

    Google Scholar 

  • Pauvert P and [ptde la} Tullaye B (1977) Etude des conditions de l’orge par l’oidium et la période de latence chez Erysiphe graminis f.sp. hordei. Ann Phytopathol 9: 495–501

    Google Scholar 

  • Pedersen LH (1992). PhD thesis. Plant Biology Section, Risø National Laboratory, Denmark and Dept. Biochem. Nutrition, Danish Technical University.

    Google Scholar 

  • Rasmussen M, Rossen L, Giese H (1993) SINE-like properties of a highly repetitive element in the genome of the obligate parasitic fungus Erysiphe graminis f.sp. hordei. Mol Gen Genet 239: 298–303

    CAS  Google Scholar 

  • Russo VM and Bushnell WR (1989) Responses of barley cells to puncture by microneedles and to attempted penetration by Erysiphe graminis f.sp. hordei. Can J Bot 67: 2912–2921

    Google Scholar 

  • Schwarzbach E (1979) Response to selection for virulence against the ml-o based mildew resistance in barley, not fitting the gene-for-gene hypothesis. Barley Genet Newsl 9: 85–88

    Google Scholar 

  • Scott-Craig JS, Kerby KB, Stein BD and Somerville SC (1995) Expression of an extracellular peroxidase that is induced in barley (Hordeum vulgare) by the powdery mildew pathogen (Erysiphe graminis f.sp. hordei). Physiol Mol Plant Pathol 47: 407–418

    CAS  Google Scholar 

  • Sherwood JE and Somerville SC (1990) Sequence of the Erysiphe graminis f.sp. hordei gene encoding ?-tubulin. Nucl Acids Res 18: 1052

    PubMed  CAS  Google Scholar 

  • Shiraishi T, Yamaoka N and Kunoh H (1989) Association between increased Phenylalanine ammonia lyase activity and cinnamic acid synthesis and the induction of temporary inaccessibility caused by Erysiphe graminis primary germ tube penetration of the barley leaf. Physiol Mol Plant Pathol 34: 75–83

    CAS  Google Scholar 

  • Skou JP, Jørgensen JH and Lilholt U (1984) Comparative studies of callose formation in powdery mildew compatible and incompatible barley. Phytopathol Z 109: 147–168

    Google Scholar 

  • Smart MG, Aist JR and Israel HW (1986) Structure and function of wall appositions. 1. General histochemistry of paillae in barley coleoptiles attacked by Erysiphe graminis f.sp. hordei. Can J Bot 64: 793–801

    CAS  Google Scholar 

  • Smith SE and Smith FA (1990) Structure and function of the interface in biotrophic symbioses as they relate to nutrient transport. New Phytol 114: 1–38

    CAS  Google Scholar 

  • Speer EO (1973) Untersuchungen zur Morphologie und Systematik der Erysiphacen. I. Die Gattung Blumeria Golovin und ihre Typusart Erysiphe graminis DC. Sydowia 27:1–6

    Google Scholar 

  • Spencer-Phillips PTN and JL Gay (1981) Domains of ATPase in plasma membranes and transport through infected plant cells. New Phytol 89: 393–400

    CAS  Google Scholar 

  • Stanbridge B, Gay JL and Wood RKS (1971) Gross and fine structural changes in Erysiphe graminis and barley before and during infection. In: Preece TF and Dickinson CH (eds) Ecology of Leaf Surface Micro-Organisms, pp 367–379. Academic Press, London

    Google Scholar 

  • Staub T, Dahmen H and Schwinn FJ (1974) Light-and scanning electron microscopy of cucumber and barley powdery mildew on host and nonhost plants. Phytopathol 64: 364–372

    Google Scholar 

  • Takahashi K, Aist JR and Israel HW (1985) Distribution of hydrolytic enzymes at barley powdery mildew encounter sites: implications for resistance associated with papilla formation in a compatible system. Physiol Plant Pathol 27: 167–184

    CAS  Google Scholar 

  • Thordal-Christensen H, Brandt J, Cho BH, Gregersen PL, Rasmussen SK, Smedegaard-Petersen V and Collinge DB (1992) cDNA cloning and characterization of two barley peroxidase transcripts induced differentially by the powdery mildew fungus Erysiphe graminis. Physiol Mol Plant Pathol 40: 395–409

    CAS  Google Scholar 

  • Thordal-Christensen H and Smedegaard-Petersen V (1988a) Comparison of resistance-inducing abilities of virulent and avirulent races of Erysiphe graminis f.sp. hordei and a race of Erysiphe graminis f.sp. tritici. Plant Pathol 37 20–27

    Google Scholar 

  • Thordal-Christensen H and Smedegaard-Petersen V (1988b) Correlation between induced resistance and host fluorescence in barley inoculated with Erysiphe graminis. J Phytopathol 123 34–46

    Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei YD and Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187–1194

    CAS  Google Scholar 

  • Torp J and Jørgensen JH (1986) Modification of barley powdery mildew resistance gene MI-a12 by induced mutation. Can J Genet Cytol 28: 725–731

    Google Scholar 

  • Tosa Y and Shishiyama J (1984) Cytological aspects of events occuring after the formation of primary haustoria in barley leaves infected with powdery mildew. Can J Bot 62: 795–798

    Google Scholar 

  • Walther-Larsen H, Brandt J, Collinge DB and Thordal-Christensen H (1993) A pathogen-induced gene of barley encodes a HSP90 homologue showing striking similarity to vertebrate forms resident in the endoplasmic reticulum. Plant Mol Biol 21: 1097–1108

    PubMed  CAS  Google Scholar 

  • Wei YD, de Neergaard E, Thordal-Christensen H, Collinge DB and Smedegaard-Petersen V (1994) Accumulation of a putative guanidine compound in relation to other early defence reactions in epidermal cells of barley and wheat exhibiting resistance to Erysiphe graminis f.sp. hordei. Physiol Mol Plant Pathol 45: 469–484

    CAS  Google Scholar 

  • Wei YD, Collinge DB, Smedegaard-Petersen V and Thordal-Christensen H (1996) Characterization of the transcript of a new class of retroposon-type repetitive element cloned from the powdery mildew fungus, Erysiphe graminis. Mol Gen Genet 250: 477–482

    PubMed  CAS  Google Scholar 

  • Wei YD, Zhang Z, Andersen CH, Schmelzer E, Gregersen PL, Collinge DB, Smedegaard-Petersen V and Thordal-Christensen H (1998) An epidermis/papilla-specific Oxalate oxidase-like protein in the defence response of barley attacked by the powdery mildew fungus. Plant Mol Biol 36: 101–112

    PubMed  CAS  Google Scholar 

  • Wolfe MS and McDermott JM (1994) Population genetics of plant pathogen interactions: the example of the Erysiphe graminis — Hordeum vulgare pathosystem. Ann Rev Phytopathol 32: 89–113

    Google Scholar 

  • Woolacott B and Archer SA (1984) The influence of the primary germ tube on infection of barley by Erysiphe graminis f.sp. hordei. Plant Pathol 33: 225–231

    Google Scholar 

  • Wright AJ and Heale JB (1988) Host responses to fungal penetration in Erysiphe graminis f.sp. hordei infections in barley. Plant Pathol 37: 131–140

    Google Scholar 

  • Yarwood CE (1978) History and taxonomy of powdery mildew. In: Spencer DM (ed) The Powdery Mildews, pp 1–37. Academic Press, London

    Google Scholar 

  • Zeyen RJ, Carver TLW and Ahlstrand GG (1983) Relating cytoplasmic detail of powdery mildew infection to presence of insoluble silicon by sequential use of light microscopy, SEM, and X-ray microanalysis. Physiol Plant Pathol 22: 101–108

    CAS  Google Scholar 

  • Zhang Z, Collinge DB and Thordal-Christensen H (1995) Germin-like Oxalate oxidase, a H2O2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J 8: 139–145

    CAS  Google Scholar 

  • Zhou F, Zhang, Z, Gregersen PL, Mikkelsen JD, de Neergaard E, Collinge DB and Thordal-Christensen (1998) Molecular characterization of the Oxalate oxidase involved in the response of barley to the powdery mildew fungus. Plant Physiol 117: 33–41

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Plant Pathology and Biogeochemistry Department, Risoe National Laboratory, DK-4000, Roskilde, Denmark

    Hans Thordal-Christensen

  2. Plant Pathology Section, Department of Plant Biology, The Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871, Frederiksberg C, Copenhagen, Denmark

    Per L. Gregersen & David B. Collinge

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  1. Hans Thordal-Christensen
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  2. Per L. Gregersen
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  3. David B. Collinge
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Editors and Affiliations

  1. RWTH, Aachen, Germany

    A. J. Slusarenko

  2. Society for General Microbiology, Reading, UK

    R. S. S. Fraser (Honorary Visiting Professor) (Honorary Visiting Professor)

  3. Utrecht University, The Netherlands

    L. C. van Loon

  4. University of Manchester, UK

    R. S. S. Fraser (Honorary Visiting Professor) (Honorary Visiting Professor)

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Thordal-Christensen, H., Gregersen, P.L., Collinge, D.B. (2000). The Barley/Blumeria (Syn. Erysiphe) Graminis Interaction. In: Slusarenko, A.J., Fraser, R.S.S., van Loon, L.C. (eds) Mechanisms of Resistance to Plant Diseases. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-3937-3_4

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