Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Resistance to cereal rusts at the plant cell wall—what can we learn from other host-pathogen systems?

N. C. Collins A D , R. E. Niks B and P. Schulze-Lefert C
+ Author Affiliations
- Author Affiliations

A Sainsbury Laboratory, John Innes Centre, Norwich NR4 7UH, UK; current address: Australian Centre for Plant Functional Genomics, PMB1 Glen Osmond, SA 5064, Australia.

B Department of Plant Breeding, Wageningen University, PO Box 386, 6700 Wageningen, The Netherlands.

C Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Carl von Linné Weg 10, D-50829 Köln, Germany.

D Corresponding author. Email: nick.collins@acpfg.com.au

Australian Journal of Agricultural Research 58(6) 476-489 https://doi.org/10.1071/AR06065
Submitted: 1 March 2006  Accepted: 25 July 2006   Published: 26 June 2007

Abstract

The ability of plant cells to resist invasion by pathogenic fungi at the cell periphery (pre-invasion resistance) differs from other types of resistance that are generally triggered after parasite entry and during differentiation of specialised intracellular feeding structures. Genetic sources of pre-invasion resistance such as mlo for barley powdery mildew and Lr34 for resistance to wheat leaf rust have proven to be broad-spectrum in effect and durable in the field. Continued breeding for this type of resistance (often quantitative in effect) is therefore considered an important strategy to protect cereal crops long-term against potentially devastating fungal diseases such as rusts. Considerable progress has been made in characterising genes and processes underlying pre-invasion resistance using mutant analysis, molecular genetics, gene cloning, and the model plant Arabidopsis, as well as comparative functional analysis of genes in Arabidopsis and cereals. This review summarises the current knowledge in this field, and discusses several aspects of pre-invasion resistance potentially pertinent to use in breeding; namely, biological cost of the resistance and effectiveness of individual resistance genes against multiple pathogen types. We show that mutations in Mlo, Ror1, and Ror2 genes known to affect powdery mildew pre-invasion resistance have no detectable effect on partial resistance to barley leaf rust as measured by latency period.

Additional keywords: Lr46, Sr2, PEN genes, partial resistance, pre-haustorial resistance.


Acknowledgments

NC was supported by Syngenta and the Gatsby Foundation at the Sainsbury Laboratory. The authors gratefully thank T. Schnurbusch for helpful comments, and T. Carver (IGER, Aberystwyth) and Rosemary White (CSIRO, Canberra) for kindly providing Fig. 1a and 1b, respectively.


References


Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell 16, 3460–3479.
CrossRef | PubMed |

Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L , et al. (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Molecular Biology of the Cell 15, 5118–5129.
CrossRef | PubMed |

Berbee ML (2001) The phylogeny of plant and animal pathogens in the Ascomycota. Physiological and Molecular Plant Pathology 59, 165–187.
CrossRef |

Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proceedings of the National Academy of Sciences of the United States of America 102, 3135–3140.
CrossRef | PubMed |

Bjørnstad Å, Aastveit K (1990) Pleiotropic effects on the Ml-o mildew resistance gene in barley in different genetic backgrounds. Euphytica 46, 217–226.
CrossRef |

Bonin CP, Potter I, Vanzin GF, Reiter WD (1997) The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose. Proceedings of the National Academy of Sciences of the United States of America 94, 2085–2090.
CrossRef | PubMed |

Brown JKM (2002) Yield penalties of disease resistance in crops. Current Opinion in Plant Biology 5, 339–344.
CrossRef | PubMed |

Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, vanDaelen R, vander Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88, 695–705.
CrossRef | PubMed |

Caldwell KS, Russell J, Langridge P, Powell W (2006) Extreme population dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare. Genetics 172, 557–567.
CrossRef | PubMed |

Christensen AB, Thordal-Christensen H, Zimmermann G, Gjetting T, Lyngkjær MF, Dudler R, Schweizer P (2004) The germinlike protein GLP4 exhibits superoxide dismutase activity and is an important component of quantitative resistance in wheat and barley. Molecular Plant-Microbe Interactions 17, 109–117.
CrossRef | PubMed |


Collins NC, Lahaye T, Peterhänsel C, Freialdenhoven A, Corbitt M, Schulze-Lefert P (2001) Sequence haplotypes revealed by sequence-tagged site fine mapping of the Ror1 gene in the centromeric region of barley chromosome 1H. Plant Physiology 125, 1236–1247.
CrossRef | PubMed |

Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E , et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973–977.
CrossRef | PubMed |

Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J , et al. (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nature Genetics 38, 716–720.
CrossRef | PubMed |

Craig S, Beaton CD (1996) A simple cryo-SEM method for delicate plant tissues. Journal of Microscopy 182, 102–105.
CrossRef |

Devoto A, Hartmann HA, Piffanelli P, Elliott C, Simmons C , et al. (2003) Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. Journal of Molecular Evolution 56, 77–88.
CrossRef | PubMed |

Devoto A, Piffanelli P, Nilsson I, Wallin E, Panstruga R, von Heijne G, Schulze-Lefert P (1999) Topology, subcellular localization, and sequence diversity of the Mlo family in plants. The Journal of Biological Chemistry 274, 34993–35004.
CrossRef | PubMed |

Dong XN (2004) NPR1, all things considered. Current Opinion in Plant Biology 7, 547–552.
CrossRef | PubMed |

Douchkov D, Nowara D, Zierold U, Schweizer P (2005) A high-throughput gene-silencing system for the functional assessment of defense-related genes in barley epidermal cells. Molecular Plant-Microbe Interactions 18, 755–761.
CrossRef | PubMed |


Dreiseitl A, Dinoor A (2004) Phenotypic diversity of barley powdery mildew resistance sources. Genetic Resources and Crop Evolution 51, 251–257.
CrossRef |

Elliott C, Zhou FS, Spielmeyer W, Panstruga R, Schulze-Lefert P (2002) Functional conservation of wheat and rice Mlo orthologs in defense modulation to the powdery mildew fungus. Molecular Plant-Microbe Interactions 15, 1069–1077.
CrossRef | PubMed |


Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, Cabral A, Parker JE (2005) Arabidopsis senescence–associated gene101 stabilizes and signals within an enhanced disease susceptibility1 complex in plant innate immunity. The Plant Cell 17, 2601–2613.
CrossRef | PubMed |

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

Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis.  Molecular Cell 5, 1003–1011.
CrossRef | PubMed |

Görlach J, Volrath S, KnaufBeiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. The Plant Cell 8, 629–643.
CrossRef | PubMed |

Hardham AR, Mitchell HJ (1998) Use of molecular cytology to study the structure and biology of phytopathogenic and mycorrhizal fungi. Fungal Genetics and Biology 24, 252–284.
CrossRef | PubMed |

Hare RA, McIntosh RA (1979) Genetic and cytogenetic studies of durable adult-plant resistance in ‘Hope’ and related cultivars to wheat rusts. Zeitschrift für Pflanzenzüchtung 83, 350–367.

Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Annals of Botany 80, 713–720.
CrossRef |

Heil M (2002) Ecological costs of induced resistance. Current Opinion in Plant Biology 5, 345–350.
CrossRef | PubMed |

Heil M, Hilpert A, Kaiser W, Linsenmair KE (2000) Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology 88, 645–654.
CrossRef |

Hoogkamp TJH, Chen WQ, Niks RE (1998) Specificity of prehaustorial resistance to Puccinia hordei and to two inappropriate rust fungi in barley. Phytopathology 88, 856–861.
CrossRef |


Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. The Plant Cell 15, 2503–2513.
CrossRef | PubMed |

Jahn R, Lang T, Sudhof TC (2003) Membrane fusion. Cell 112, 519–533.
CrossRef | PubMed |

Jarosch B, Collins NC, Zellerhoff N, Schaffrath U (2005) RAR1, ROR1, and the actin cytoskeleton contribute to basal resistance to Magnaporthe grisea in barley. Molecular Plant-Microbe Interactions 18, 397–404.
CrossRef | PubMed |


Jarosch B, Kogel KH, 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. Molecular Plant-Microbe Interactions 12, 508–514.
CrossRef |


Jørgensen JH (1977) Spectrum of resistance conferred by ML-O powdery mildew resistance genes in barley. Euphytica 26, 55–62.
CrossRef |

Jørgensen JH (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63, 141–152.
CrossRef |

Jørgensen JH (1994) Genetics of powdery mildew resistance in barley. Critical Reviews in Plant Sciences 13, 97–119.
CrossRef |


Kim MC, Panstruga R, Elliott C, Muller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P (2002) Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416, 447–450.
CrossRef | PubMed |

Kjær B, Jensen HP, Jensen J, Jørgensen JH (1990) Associations between 3 Ml-O powdery mildew resistance genes and agronomic traits in barley. Euphytica 46, 185–193.
CrossRef |

Kobayashi I, Kobayashi Y, Hardham AR (1994) Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195, 237–247.
CrossRef |

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

Kobayashi Y, Yamada M, Kobayashi I, Kunoh H (1997b) Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant & Cell Physiology 38, 725–733.

Kogel KH, Langen G (2005) Induced disease resistance and gene expression in cereals. Cellular Microbiology 7, 1555–1564.
CrossRef | PubMed |

Koh S, André A, Edwards H, Ehrhardt D, Somerville S (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. The Plant Journal 44, 516–529.
CrossRef | PubMed |

Kota R, Spielmeyer W, McIntosh RA, Lagudah ES (2006) Fine genetic mapping fails to dissociate durable stem rust resistance gene Sr2 from pseudo-black chaff in common wheat (Triticum aestivum L.). Theoretical and Applied Genetics 112, 492–499.
CrossRef | PubMed |

Kumar J, Hückelhoven R, Beckhove U, Nagarajan S, Kogel KH (2001) A compromised Mlo pathway affects the response of barley to the necrotrophic fungus Bipolaris sorokiniana (Teleomorph: Cochliobolus sativus) and its toxins. Phytopathology 91, 127–133.
CrossRef |


Kunoh H, Hayashimoto A, Harui M, Ishizaki H (1985) Induced susceptibility and enhanced resistance at the cellular-level in barley coleoptiles. I. The significance of timing of fungal invasion. Physiological Plant Pathology 27, 43–54.

Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M , et al. (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310, 1180–1183.
CrossRef | PubMed |

Lyngkjær HF, Carver TLW (1999) Modification of mlo5 resistance to Blumeria graminis attack in barley as a consequence of induced accessibility and inaccessibility. Physiological and Molecular Plant Pathology 55, 163–174.
CrossRef |

Lyngkjær MF, Jensen HP, Ostergard H (1995) A Japanese powdery mildew isolate with exceptionally large infection efficiency on Mlo-resistant barley. Plant Pathology 44, 786–790.
CrossRef |

Martínez F, Niks RE, Singh RP, Rubiales D (2001) Characterization of Lr46, a gene conferring partial resistance to wheat leaf rust. Hereditas 135, 111–114.
CrossRef | PubMed |

Matsumura K, Tosa Y (1995) The rye mildew fungus carries avirulence genes corresponding to wheat genes for resistance to races of the wheat mildew fungus. Phytopathology 85, 753–756.
CrossRef |

McIntosh RA , Wellings CR , Park RF (1995) ‘Wheat rusts: an atlas of resistance genes.’ (CSIRO Publishing: Melbourne, Vic.)

Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. The Plant Journal 29, 257–268.
CrossRef | PubMed |

Mellersh DG, Heath MC (2001) Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. The Plant Cell 13, 413–424.
CrossRef | PubMed |

Mellersh DG, Heath MC (2003) An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. Molecular Plant-Microbe Interactions 16, 398–404.
CrossRef | PubMed |


Niks RE (1983) Haustorium formation by Puccinia hordei in leaves of hypersensitive, partially resistant, and non-host plant genotypes. Phytopathology 73, 64–66.

Niks RE (1986) Failure of haustorial development as a factor in slow growth and development of Puccinia hordei in partially resistant barley seedlings. Physiological and Molecular Plant Pathology 28, 309–322.

Niks RE (1988) Nonhost plant-species as donors for resistance to pathogens with narrow host range. 2. Concepts and evidence on the genetic-basis of nonhost resistance. Euphytica 37, 89–99.
CrossRef |

Niks RE (1989) Induced accessibility and inaccessibility of barley cells in seedling leaves inoculated with two leaf rust species. Journal of Phytopathology 124, 296–308.

Niks RE, Rubiales D (2002) Potentially durable resistance mechanisms in plants to specialised fungal pathogens. Euphytica 124, 201–216.
CrossRef |

Niks RE, Walther U, Jaiser H, Martínez F, Rubiales D , et al. (2000) Resistance against barley leaf rust (Puccinia hordei) in West-European spring barley germplasm. Agronomie 20, 769–782.
CrossRef |

Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301, 969–972.
CrossRef | PubMed |

Opalski KS, Schultheiss H, Kogel KH, Hückelhoven R (2005) The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f. sp. hordei. The Plant Journal 41, 291–303.
CrossRef | PubMed |

Panstruga R, Schulze-Lefert P (2003) Corruption of seven-transmembrane proteins by pathogenic microbes: a common theme in animals and plants? Microbes and Infection 5, 429–437.
CrossRef | PubMed |

Peterhänsel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze-Lefert P (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. The Plant Cell 9, 1397–1409.
CrossRef | PubMed |

Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D’Hont A, Hollricher K, Jørgensen JH, Schulze-Lefert P, Panstruga R (2004) A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430, 887–891.
CrossRef | PubMed |

Piffanelli P, Zhou FS, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiology 129, 1076–1085.
CrossRef | PubMed |

Qi X, Jiang G, Chen W, Niks RE, Stam P, Lindhout P (1999) Isolate-specific QTLs for partial resistance to Puccinia hordei in barley. Theoretical and Applied Genetics 99, 877–884.
CrossRef |

Qi X, Niks RE, Stam P, Lindhout P (1998a) Identification of QTLs for partial resistance to leaf rust (Puccinia hordei) in barley. Theoretical and Applied Genetics 96, 1205–1215.
CrossRef |

Qi X, Stam P, Lindhout P (1998b) Use of locus-specific AFLP markers to construct a high-density molecular map in barley. Theoretical and Applied Genetics 96, 376–384.
CrossRef |

Reuhs BL, Glenn J, Stephens SB, Kim JS, Christie DB, Glushka JG, Zablackis E, Albersheim P, Darvill AG, O’Neill MA (2004) L-Galactose replaces L-fucose in the pectic polysaccharide rhamnogalacturonan II synthesized by the L-fucose-deficient mur1 Arabidopsis mutant. Planta 219, 147–157.
CrossRef | PubMed |

Rodrigues P, Garrood JM, Shen QH, Smith PH, Boyd LA (2004) The genetics of non-host disease resistance in wheat to barley yellow rust. Theoretical and Applied Genetics 109, 425–432.
CrossRef | PubMed |

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. The Journal of Biological Chemistry 273, 9013–9022.
CrossRef | PubMed |

Rosewarne GM, Singh RP, Huerta-Espino J, William HM, Bouchet S, Cloutier S, McFadden H, Lagudah ES (2006) Leaf tip necrosis, molecular markers and β1-proteasome subunits associated with the slow rusting resistance genes Lr46/Yr29. Theoretical and Applied Genetics 112, 500–508.
CrossRef | PubMed |

Rubiales D, Niks RE (1995) Characterization of Lr34, a major gene conferring non-hypersensitive resistance to wheat leaf rust. Plant Disease 79, 1208–1212.

Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter WD, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiology 132, 1033–1040.
CrossRef | PubMed |

Schmelzer E (2002) Cell polarization, a crucial process in fungal defence. Trends in Plant Science 7, 411–415.
CrossRef | PubMed |

Schnurbusch T, Bossolini E, Messmer M, Keller B (2004a) Tagging and validation of a major quantitative trait locus for leaf rust resistance and leaf tip necrosis in winter wheat cultivar Forno. Phytopathology 94, 1036–1041.
CrossRef |


Schnurbusch T, Paillard S, Schori A, Messmer M, Schachermayr G, Winzeler M, Keller B (2004b) Dissection of quantitative and durable leaf rust resistance in Swiss winter wheat reveals a major resistance QTL in the Lr34 chromosomal region. Theoretical and Applied Genetics 108, 477–484.
CrossRef | PubMed |

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 Genetics Newsletter 9, 85–88.

Shen QH, Zhou FS, 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.
CrossRef | PubMed |

Singh RP (1992a) Association between gene Lr34 for leaf rust resistance and leaf tip necrosis in wheat. Crop Science 32, 874–878.

Singh RP (1992b) Genetic association of leaf rust resistance gene Lr34 with adult-plant resistance to stripe rust in bread wheat. Phytopathology 82, 835–838.

Singh RP, Burnett PA, Albarran M, Rajaram S (1993) Bdv1—a gene for tolerance to barley yellow dwarf virus in bread wheats. Crop Science 33, 231–234.

Singh RP, Huerta-Espino J (1997) Effect of leaf rust resistance gene Lr34 on grain yield and agronomic traits of spring wheat. Crop Science 37, 390–395.

Singh RP, Mcintosh RA (1984) Complementary genes for reaction to Puccinia recondita tritici in Triticum aestivum. 1. Genetic and linkage studies. Canadian Journal of Genetics and Cytology 26, 723–735.

Singh RP, Mujeeb-Kazi A, Huerta-Espino J (1998) Lr46: A gene conferring slow rusting resistance to leaf rust in wheat. Phytopathology 88, 890–894.
CrossRef |


Singh RP, Nelson JC, Sorrells ME (2000) Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Science 40, 1148–1155.

Skou JP, Jørgensen JH, Lilholt U (1984) Comparative studies on callose formation in powdery mildew compatible and incompatible barley. Journal of Phytopathology 109, 147–168.

Snyder BA, Nicholson RL (1990) Synthesis of phytoalexins in Sorghum as a site-specific response to fungal ingress. Science 248, 1637–1639.
CrossRef |

Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005) Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theoretical and Applied Genetics 111, 731–735.
CrossRef | PubMed |

Stam P , Bos I , Qi X , Niks RE (1997) QTL mapping of yield and yield-related traits in a wide cross of spring barley (Hordeum vulgare L.). In ‘Advances in biometrical genetics. Proceedings of the 10th Meeting of the EUCARPIA Section Biometrics in Plant Breeding’. Poznań, Poland. (Eds P Krajewski, Z Kaczmarek) pp. 277–280. (Institute of Plant Genetics, Polish Academy of Sciences: Poznan, Poland)

Stein M, Dittgen J, Sánchez-Rodríguez C, Hou B-H, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. The Plant Cell 18, 731–746.
CrossRef | PubMed |

Stolzenburg MC, Aist JR, Israel HW (1984) The role of papillae in resistance to powdery mildew conditioned by the Ml-O gene in barley. 1. Correlative evidence. Physiological Plant Pathology 25, 337–346.

Thomas WTB, Baird E, Fuller JD, Lawrence P, Young GR, Russell J, Ramsay L, Waugh R, Powell W (1998) Identification of a QTL decreasing yield in barley linked to Mlo powdery mildew resistance. Molecular Breeding 4, 381–393.
CrossRef |

Thordal-Christensen H, Zhang ZG, Wei YD, Collinge DB (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.
CrossRef |

Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74–77.
CrossRef | PubMed |

Tosa Y, Shishiyama J (1984) Defense reactions of barley cultivars to an inappropriate forma specialis of the powdery mildew fungus of gramineous plants. Canadian Journal of Botany 62, 2114–2117.

Vogel J, Somerville S (2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proceedings of the National Academy of Sciences of the United States of America 97, 1897–1902.
CrossRef | PubMed |

Wei YD, Zhang ZG, Andersen CH, Schmelzer E, Gregersen PL, Collinge DB, Smedegaard-Petersen V, 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 Molecular Biology 36, 101–112.
CrossRef | PubMed |

Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Current Opinion in Plant Biology 8, 383–389.
CrossRef | PubMed |

William M, Singh RP, Huerta-Espino J, Islas SO, Hoisington D (2003) Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat. Phytopathology 93, 153–159.
CrossRef |


Wolter M, Hollricher K, Salamini F, Schulze-Lefert P (1993) The Mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defense mimic phenotype. Molecular & General Genetics 239, 122–128.

Xu ZW, Escamilla-Trevino LL, Zeng LH, Lalgondar M, Bevan DR , et al. (2004) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Molecular Biology 55, 343–367.
CrossRef | PubMed |

Yun BW, Atkinson HA, Gaborit C, Greenland A, Read ND, Pallas JA, Loake GJ (2003) Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. The Plant Journal 34, 768–777.
CrossRef | PubMed |

Zeyen RJ, Bushnell WR (1979) Papilla response of barley epidermal cells caused by Erysiphe graminis: rate and method of deposition determined by microcinematography and transmission microscopy. Canadian Journal of Botany 57, 898–913.

Zeyen RJ , Carver TLW , Lyngkjær MF (2002) Epidermal cell papillae. In ‘The powdery mildews. A comprehensive treatise’. (Eds RR Bélanger, WR Bushnell, AJ Dik, TLW Carver) pp. 107–125. (American Phytopathological Society: St. Paul, MN)

Zierold U, Scholz U, Schweizer P (2005) Transcriptome analysis of mlo-mediated resistance in the epidermis of barley. Molecular Plant Pathology 6, 139–151.
CrossRef |

Zimmerli L, Stein M, Lipka V, Schulze-Lefert P, Somerville S (2004) Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. The Plant Journal 40, 633–646.
CrossRef | PubMed |

Zipfel C, Felix G (2005) Plants and animals: a different taste for microbes? Current Opinion in Plant Biology 8, 353–360.
CrossRef | PubMed |








Rent Article (via Deepdyve) Export Citation Cited By (13)