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Diversity of defence mechanisms in plant–oomycete interactions: a case study of Lactuca spp. and Bremia lactucae

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Abstract

Plant pathogenic oomycetes, including biotrophic downy mildews and hemibiotrophs/necrotrophs such as Phytophthora and Pythium, cause enormous economic losses on cultivated crops. Lettuce breeders and growers face the threat of Bremia lactucae, the causal agent of lettuce downy mildew. This pathogen damages leaf tissues and lettuce heads and is also frequent on wild Asteraceae plants. The interactions of Lactuca spp. with B. lactucae (abbr. lettuce–Bremia) display extreme variability, due to a long co-evolutionary history. For this reason, during the last 30 years, the lettuce–Bremia pathosystem has been used as a model for many studies at the population, individual, organ, tissue, cellular, physiological and molecular levels, as well as on genetic variability and the genetics of host–parasite interactions. The first part of this review summarizes recent data on host–parasite specificity, host variability, resistance mechanisms and genetics of lettuce–Bremia interactions. The second part focuses on the development infection structures. Phenotypic expression of infection, behaviour of B. lactucae on leaf surfaces, the process of penetration, development of primary infection structures, hyphae and haustoria are discussed in relation to different resistance mechanisms. In the third part, the components of host resistance and the variability of defence responses are analysed. The role of reactive oxygen species (ROS), antioxidant enzymes, nitric oxide (NO), phenolic compounds, reorganization of cytoskeleton, electrolyte leakage, membrane damage, cell wall disruption, hypersensitive reaction and plant energetics are discussed in relation to defence responses. In general, the extreme variability of interactions between lettuce and Bremia, and their phenotypic expression, results from diversity of the genetic background. Different mechanisms of resistance are conditioned by an orchestra of defence responses at the tissue, cell, and molecular levels. The various events responsible for defence involve a complex interaction of the processes and reactions mentioned above. This review also provides an overview on the timing of pathogen development, host pathological anatomy, cytology and physiology of lettuce–Bremia associations. The significance of these factors on the expression of different resistance mechanisms (non-host and host resistance, race-specific and race non-specific resistance, field resistance) is discussed.

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Abbreviations

ATP:

adenosine triphosphate

BAP:

benzylaminopurine

CKs:

cytokinins

dai:

days after inoculation

EHM:

extrahaustorial membrane

ER:

endoplasmatic reticulum

H:

intercellular hypha

HA:

haustorium

hai:

hours after inoculation

HR:

hypersensitive reaction

IH:

intracellular hypha

IMD:

irreversible membrane damage

MTs:

microtubules

NADPH:

reduced nicotinamide adenine dinucleotide phophate

NO:

nitric oxide

NOS:

nitric oxide synthase

PAL:

phenylalanine ammonium lyase

PAs:

phenolic acids

POX:

peroxidase

PSII:

photosystem II

PTIO:

2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide

QTL:

quantitative trait loci

ROS:

reactive oxygen species

TEM:

transmission electron microscopy

3-MeOBAPR:

6-(3-methoxy-benzylamino)purine-9-β-ribofuranoside

References

  • Aguirreolea, J., Irigoyen, J., Sanchez-Diaz, M., & Salaverri, J. (1995). Physiological alterations in pepper during wilt induced by Phytophthora capsici and soil water deficit. Plant Pathology, 44, 587–596.

    Article  Google Scholar 

  • Andrews, J. H. (1975). Distribution of label from 3H-glucose and 3H-leucine in lettuce cotyledons during the early stages of infection with Bremia lactucae. Canadian Journal of Botany, 53, 1103–1115.

    CAS  Google Scholar 

  • Beharav, A., Lewinsohn, D., Lebeda, A., & Nevo, E. (2006). New wild Lactuca genetic resources with resistance against Bremia lactucae. Genetic Resources and Crop Evolution, 53, 467–474.

    Article  Google Scholar 

  • Bennett, M., Gallagher, M., Fagg, J., Bestwick, C., Paul, T., Beale, M., et al. (1996). The hypersensitive reaction, membrane damage and accumulation of autofluorescence phenolics in lettuce cells challenged by Bremia lactucae. The Plant Journal, 9, 851–865.

    Article  CAS  Google Scholar 

  • Bestwick, C. S., Adam, A. L., Puri, N., & Mansfield, J. W. (2001). Characterisation of changes to pro- and anti-oxidant enzyme activities during the hypersensitive reaction in lettuce (Lactuca sativa L.). Plant Science, 161, 497–506.

    Article  CAS  Google Scholar 

  • Binet, M. N., Humbert, C., Lecourieux, D., Vantard, M., & Pugin, A. (2001). Disruption of microtubular cytoskeleton induced by cryptogein, an elicitor of hypersensitive response in tobacco cells. Plant Physiology, 125, 564–572.

    Article  PubMed  CAS  Google Scholar 

  • Birch, P. R. J., Rehmany, A. P., Pritchard, L., Kamoun, S., & Beynon, J. L. (2006). Trafficking arms: Oomycete effectors enter host plant cells. Trends in Microbiology, 14, 8–11.

    Article  PubMed  CAS  Google Scholar 

  • Bohm, B. A., & Stuessy, T. F. (2001). Flavonoids of the sunflower family (Asteraceae). Wien: Springer.

    Google Scholar 

  • Bonnier, F. J. M., Reinink, K., & Groenwold, R. (1994). Genetic analysis of Lactuca accessions with new major gene resistance to lettuce downy mildew. Phytopathology, 84, 462–468.

    Article  Google Scholar 

  • Carzaniga, R., Bowyer, P., & O’Connell, R. J. (2001). Production of extracellular matrices during development of infection structures by the downy mildew Peronospora parasitica. New Phytologist, 149, 83–93.

    Article  CAS  Google Scholar 

  • Chen, Y. H., Chen, H. Y., Hsu, C. L., & Yen, G. C. (2007). Induction of apoptosis by Lactuca indica L. in human leukemia cell line and its active components. Journal of Agricultural and Food Chemistry, 55, 1743–1749.

    Article  PubMed  CAS  Google Scholar 

  • Choi, Y. J., Hong, S. B., & Shin, H. D. (2007). Extreme size and sequence variation in the ITS rDNA of Bremia lactucae. Mycopathologia, 163, 91–95.

    Article  PubMed  CAS  Google Scholar 

  • Clark, J. S. C., & Spencer-Phillips, P. T. N. (2004). The compatible interaction in downy mildew infections. In P. T. N. Spencer-Phillips, & M. Jeger (Eds.) Advances in downy mildew research, vol. 2 (pp. 1–34). Dordrecht: Kluwer.

    Google Scholar 

  • Cohen, Y., Rubin, E., & Gotlieb, D. (2008). Activity of carboxylic acid amide (CAA) fungicides against Bremia lactucae. European Journal of Plant Pathology (this issue).

  • Crute, I. R. (1992a). Downy mildew of lettuce. In H. S. Chaube, J. Kumar, A. N. Mukhopadhyay, & U. S. Singh (Eds.) Plant diseases of international importance, vol. II. Diseases of vegetable and oil seed crops (pp. 165–185). New Jersey: Prentice Hall.

    Google Scholar 

  • Crute, I. R. (1992b). From breeding to cloning (and back again?): A case study with lettuce downy mildew. Annual Review of Phytopathology, 30, 485–506.

    Article  PubMed  CAS  Google Scholar 

  • Crute, I. R., & Dickinson, C. R. (1976). The behaviour of Bremia lactucae on cultivars of Lactuca sativa and on other Composites. Annals of Applied Biology, 82, 433–450.

    Article  Google Scholar 

  • Crute, I. R., & Dixon, G. R. (1981). Downy mildew diseases caused by the genus Bremia Regel. In D. M. Spencer (Ed.) The downy mildews (pp. 421–460). London: Academic.

    Google Scholar 

  • Crute, I. R., & Johnson, A. G. (1976). The genetic relationship between races of Bremia lactucae and cultivars of Lactuca sativa. Annals of Applied Biology, 83, 125–137.

    Article  Google Scholar 

  • Crute, I. R., & Norwood, J. M. (1981). The identification and characteristics of field resistance to lettuce downy mildew (Bremia lactucae Regel). Euphytica, 30, 707–717.

    Article  Google Scholar 

  • Davis, R. M., Subbarao, K. V., Raid, R. N., & Kurtz, E. A. (1997). Compendium of lettuce diseases. St. Paul, MN. USA: APS.

    Google Scholar 

  • Delledonne, M., Polverari, A., & Murgia, I. (2003). The functions of nitric oxide-mediated signalling and changes in gene expression during the hypersensitive response. Antioxidants and Redox Signaling, 5, 33–41.

    Article  PubMed  CAS  Google Scholar 

  • Duddridge, J. A., & Sargent, J. A. (1978). A cytochemical study of lipolytic activity in Bremia lactucae Regel during germination of the conidium and penetration of the host. Physiological Plant Pathology, 12, 289–296.

    Article  CAS  Google Scholar 

  • Fleischmann, F., Koehl, J., Portz, R., Beltrame, A. B., & Oßwald, W. F. (2005). Physiological changes of Fagus silvatica seedlings infected with Phytophthora citricola and the contribution of its elicitin “Citricolin” to pathogenesis. Plant Biology, 7, 650–658.

    Article  PubMed  CAS  Google Scholar 

  • Fleischmann, F., Schneider, D., Matyssek, R., & Oßwald, W. F. (2002). Investigation on net CO2 assimilation, transpiration and root growth of Fagus sylvatica infected with four different Phytophthora species. Plant Biology, 4, 144–152.

    Article  Google Scholar 

  • Gisi, U., & Sierotzki, H. (2008). Fungicides modes of action and resistance in downy mildews. European Journal of Plant Pathology DOI 10.1007/s10658-008-9290-5.

  • Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology, 43, 205–227.

    Article  PubMed  CAS  Google Scholar 

  • Göker, M., Voglmayr, H., Riethmüller, A., & Oberwinkler, F. (2007). How do obligate parasites evolve? A multi-gene phylogenetic analysis of downy mildews. Fungal Genetics and Biology, 44, 105–122.

    Article  PubMed  CAS  Google Scholar 

  • Grenville-Briggs, L. J., & van West, P. (2005). The biotrophic stages of oomycete–plant interactions. Advances in Applied Microbiology, 57, 217–243.

    Article  PubMed  CAS  Google Scholar 

  • Grube, R. C., & Ochoa, O. E. (2005). Comparative genetic analysis of field resistance to downy mildew in the lettuce cultivars ‘Grand Rapids’ and ‘Iceberg’. Euphytica, 142, 205–215.

    Article  Google Scholar 

  • Hamada, T. (2007). Microtubule-associated proteins in higher plants. Journal of Plant Research, 120, 79–98.

    Article  PubMed  CAS  Google Scholar 

  • Hardham, A. R. (2007). Cell biology of plant–oomycete interactions. Cellular Microbiology, 9, 31–39.

    Article  PubMed  CAS  Google Scholar 

  • Holub, E. B., & Cooper, A. (2004). Matrix, reinvention in plants: How genetics is unveiling secrets of non-host disease resistance. Trends in Plant Science, 9, 211–214.

    Article  PubMed  CAS  Google Scholar 

  • Hooftman, D. A. P., Nieuwenhuis, B. P. S., Posthuma, K. I., Oostermeijer, J. G. B., & den Nijs, H. J. C. M. (2007). Introgression potential of downy mildew resistance from lettuce to Lactuca serriola and its relevance for plant fitness. Basic and Applied Ecology, 8, 135–146.

    Article  Google Scholar 

  • Hulbert, S. H., Webb, C. A., Smith, S. M., & Sun, Q. (2001). Resistance gene complexes: Evolution and utilization. Annual Review of Phytopathology, 39, 285–312.

    Article  PubMed  CAS  Google Scholar 

  • Ingram, D. S., Sargent, J. A., & Tommerup, I. C. (1976). Structural aspects of infection by biotrophic fungi. In J. Friend & D. R. Threlfall (Eds.), Biochemical aspects of plant–parasitic relationships (pp. 43–78). Annual Proceedings of Phytochemical Society, 13.

  • Jeuken, M., & Lindhout, P. (2002). Lactuca saligna, a non-host for lettuce downy mildew (Bremia lactucae), harbors a new race-specific Dm gene and three QTLs for resistance. Theoretical and Applied Genetics, 105, 384–391.

    Article  PubMed  CAS  Google Scholar 

  • Johnstone, M., Chatterton, S., Sutton, J. C., & Grodzinski, B. (2005). Net carbon gain and growth of bell peppers, Capsicum annuum ‘Cubico’, following root infection by Pythium aphanidermatum. Phytopathology, 95, 354–361.

    Article  CAS  PubMed  Google Scholar 

  • Judelson, H. S., & Michelmore, R. W. (1992). Temperature and genotype interactions in the expression of host resistance in lettuce downy mildew. Physiological and Molecular Plant Pathology, 40, 233–245.

    Article  Google Scholar 

  • Kamoun, S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology, 44, 41–60.

    Article  PubMed  CAS  Google Scholar 

  • Kamoun, S., Huitema, E., & Vleeshouwers, V. G. A. A. (1999). Resistance to oomycetes: A general role for the hypersensitive response. Trends in Plant Science, 4, 196–200.

    Article  PubMed  Google Scholar 

  • Kitner, M., Lebeda, A., Doležalová, I., Maras, M., Křístková, E., Nevo, E., Pavlícek, T., Meglic, V., & Beharav, A. (2008). AFLP analysis of Lactuca saligna gemplasm collections from four European and three Middle East Countries. Israel Journal of Plant Sciences (in press)

  • Koch, C., Noga, G., & Strittmatter, G. (1994). Photosynthetic electron transport is differentially affected during early stages of cultivar/race-specific interactions between potato and Phytophthora infestans. Planta, 193, 551–557.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Koike, S. T., & Ochoa, O. E. (2007). Downy mildew caused by Bremia lactucae on strawflower (Helichrysum bracteatum) in California. Plant Disease, 91, 326.

    Article  Google Scholar 

  • Kuang, H., Ochoa, O. E., Nevo, E., & Michelmore, R. W. (2006). The disease resistance gene Dm3 is infrequent in natural populations of Lactuca serriola due to deletions and frequent gene conversions at the RGC2 locus. The Plant Journal, 47, 38–48.

    Article  PubMed  CAS  Google Scholar 

  • Kuang, H., Woo, S. S., Meyers, B. C., Nevo, E., & Michelmore, R. W. (2004). Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. The Plant Cell, 16, 2870–2894.

    Article  PubMed  CAS  Google Scholar 

  • Latijnhouwers, M., de Wit, P. J., & Govers, F. (2003). Oomycetes and fungi: Similar weaponry to attack plants. Trends in Microbiology, 11, 462–469.

    Article  PubMed  CAS  Google Scholar 

  • Lebeda, A. (1986). Specificity of interactions between wild Lactuca species and Bremia lactucae isolates from Lactuca serriola. Journal of Phytopathology, 117, 54–64.

    Article  Google Scholar 

  • Lebeda, A. (2002). Occurrence and variation in virulence of Bremia lactucae in natural populations of Lactuca serriola. In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.) Advances in downy mildew research (pp. 179–183). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Lebeda, A., & Boukema, I. W. (1991). Further investigation of the specificity of interactions between wild Lactuca spp. and Bremia lactucae isolates from Lactuca serriola. Journal of Phytopathology, 133, 57–64.

    Article  Google Scholar 

  • Lebeda, A., Doležalová, I., Feráková, V., & Astley, D. (2004). Geographical distribution of wild Lactuca species (Asteraceae, Lactuceae). The Botanical Review, 70, 328–356.

    Article  Google Scholar 

  • Lebeda, A., Doležalová, I., Křístková, E., Vinter, V., Vránová, O., Doležal, K., et al. (1999). Complex research of taxonomy and ecobiology of wild Lactuca spp. genetic resources. In A. Lebeda, & E. Křístková (Eds.) Eucarpia leafy vegetables ’99 (pp. 117–131). Olomouc (Czech Republic): Palacký University in Olomouc.

    Google Scholar 

  • Lebeda, A., Luhová, L., Sedlářová, M., & Jančová, D. (2001a). The role of enzymes in plant–fungal pathogens interactions. Journal of Plant Diseases and Protection, 108, 89–111.

    CAS  Google Scholar 

  • Lebeda, A., & Petrželová, I. (2004). Occurrence of race-specific resistance to Bremia lactucae in Lactuca serriola germplasm originating from four European countries. In J. Vollmann, H. Grausgruber, & P. Ruckenbauer (Eds.) Genetic variation for plant breeding (pp. (pp. 113–116)). Vienna, Austria: EUCARPIA & BOKU-University of Natural Resources and Applied Life Sciences.

    Google Scholar 

  • Lebeda, A., & Petrželová, I. (2008). Screening for resistance to lettuce downy mildew (Bremia lactucae). In M. Miranda & A. Lebeda (Eds.), Disease resistance mass screening techniques for banana and other crops. IAEA, Vienna and Springer, Dordrecht, the Netherlands (in press).

  • Lebeda, A., Petrželová, I., & Maryška, Z. (2008). Structure and variation in the wild-plant pathosystem: Lactuca serriola–Bremia lactucae. European Journal of Plant Pathology, DOI 10.1007/s10658-008-9291-4.

  • Lebeda, A., & Pink, D. A. C. (1998). Histological aspects of the response of wild Lactuca spp. and their hybrids, with L. sativa to lettuce downy mildew (Bremia lactucae). Plant Pathology, 47, 723–736.

    Google Scholar 

  • Lebeda, A., Pink, D. A. C., & Astley, D. (2002). Aspects of the interactions between wild Lactuca spp. and related genera and lettuce downy mildew (Bremia lactucae). In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.) Advances in downy mildew research (pp. 85–117). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Lebeda, A., Pink, D. A. C., & Mieslerová, B. (2001b). Host–parasite specificity and defense variability in the Lactuca spp.–Bremia lactucae pathosystem. Journal of Plant Pathology, 83, 25–35.

    CAS  Google Scholar 

  • Lebeda, A., & Reinink, K. (1991). Variation in the early development of Bremia lactucae on lettuce cultivars with different levels of field resistance. Plant Pathology, 40, 232–237.

    Article  Google Scholar 

  • Lebeda, A., & Reinink, K. (1994). Histological characterization of resistance in Lactuca saligna to lettuce downy mildew (Bremia lactucae). Physiological and Molecular Plant Pathology, 44, 125–139.

    Article  Google Scholar 

  • Lebeda, A., Ryder, E. J., Grube, R., Doležalová, I., & Křístková, E. (2007). Lettuce (Asteraceae; Lactuca spp.), Chapter 9. In R. Singh (Ed.) Genetic resources, chromosome engineering, and crop improvement series, volume 3—vegetable crops (pp. 377–472). Boca Raton, FL, USA: CRC.

    Google Scholar 

  • Lebeda, A., & Schwinn, F. J. (1994). The downy mildews—an overview of recent research progress. Journal of Plant Diseases and Protection, 101, 225–254.

    CAS  Google Scholar 

  • Lebeda, A., Sedlářová, M., Lynn, J., & Pink, D. A. C. (2006). Phenotypic and histological expression of different genetic backgrounds in interactions between lettuce, wild Lactuca spp., L. sativa × L. serriola hybrids and Bremia lactucae. European Journal of Plant Pathology, 115, 431–441.

    Article  Google Scholar 

  • Lebeda, A., & Syrovátko, P. (1988). Specificity of Bremia lactucae isolates from Lactuca sativa and some Asteraceae plants. Acta Phytopathologica et Entomologica Hungarica, 23, 39–48.

    Google Scholar 

  • Lebeda, A., & Zinkernagel, V. (2003a). Evolution and distribution of virulence in the German population of Bremia lactucae. Plant Pathology, 52, 41–51.

    Article  Google Scholar 

  • Lebeda, A., & Zinkernagel, V. (2003b). Characterization of new highly virulent German isolates of Bremia lactucae and efficiency of resistance in wild Lactuca spp. germplasm. Journal of Phytopathology, 151, 274–282.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lucas, J. A., Hayter, J. B. R., & Crute, I. R. (1995). The downy mildews: Host specificity and pathogenesis. In K. Kohmoto, U. S. Singh, & R. P. Singh (Eds.) Pathogenesis and host specificity in plant diseases (pp. 217–238). Oxford: Pergamon.

    Google Scholar 

  • MacLean, D. J., & Tommerup, I. C. (1979). Histology and physiology of compatibility between lettuce and the downy mildew fungus, Bremia lactucae Regel. Physiological Plant Pathology, 14, 291–312.

    Article  Google Scholar 

  • Mahajan, M., & Dhillon, M. (2003). Relation of leaf epidermal characteristics with susceptibility and resistance of potato (Solanum tuberosum) to late blight disease (Phytophthora infestans). Indian Journal of Agricultural Sciences, 73, 656–660.

    Google Scholar 

  • Mansfield, J. W. (2005). Biophoton distress flares signal the onset of the hypersensitive reaction. Trends in Plant Science, 10, 307–309.

    Article  PubMed  CAS  Google Scholar 

  • Mansfield, J. W., Bennett, M., Bestwick, C., & Woods-Tör, A. (1997). Phenotypic expression of gene-for-gene interaction involving fungal and bacterial pathogens: Variation from recognition to response. In I. R. Crute, E. B. Holub, & J. J. Burdon (Eds.) The gene-for-gene relationship in plant parasite interactions (pp. 265–291). Wallingford, UK: CABI.

    Google Scholar 

  • Mauch-Mani, B. (2002). Host resistance to downy mildew diseases. In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.) Advances in downy mildew research (pp. 59–83). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Mauch-Mani, B., & Slusarenko, A. J. (1996). Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell, 8, 203–212.

    Article  PubMed  CAS  Google Scholar 

  • Michelmore, R. W., & Wong, J. W. (2008). Classical and molecular genetics of Bremia lactucae, lettuce downy mildew. European Journal of Plant Pathology DOI 10.1007/s10658-008-9305-2.

  • Michelmore, R. W., Ochoa, O. E., Truco, M. J., Grube, R., & Hayes, R. (2005). Breeding crisphead lettuce. In California Lettuce Research Board Annual Report (April 1, 2004 through March 31, 2005) (pp. 68–78). Salinas, CA, USA: California Lettuce Research Board.

  • Moriondo, M., Orlandini, S., Giuntoli, A., & Bindi, M. (2005). The effect of downy and powdery mildew on grapevine (Vitis vinifera L.) leaf gas exchange. Journal of Phytopathology, 153, 350–357.

    Article  Google Scholar 

  • Neill, S. J., Desikan, R., Clarke, A., Hurst, R. D., & Hancock, J. T. (2002). Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany, 53, 1237–1247.

    Article  PubMed  CAS  Google Scholar 

  • Nordskog, B., Gadoury, D. M., Seem, R. C., & Hermansen, A. (2007). Impact of diurnal periodicity, temperature and light on sporulation of Bremia lactucae. Phytopathology, 97, 979–986.

    Article  PubMed  Google Scholar 

  • Norwood, J. M., Crute, I. R., & Lebeda, A. (1981). The utilization of novel sources of resistance to Bremia lactucae from wild Lactuca species. Euphytica, 30, 659–668.

    Article  Google Scholar 

  • O’Connell, R. J., & Panstruga, R. (2006). Tête à tête inside a plant cell: Establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytologist, 171, 699–718.

    Article  PubMed  CAS  Google Scholar 

  • Pesacreta, T. C., & Hasenstein, K. H. (1999). The internal cuticle of Cirsium horridulum (Asteraceae) leaves. American Journal of Botany, 86, 923–928.

    Article  PubMed  Google Scholar 

  • Petrželová, I., & Lebeda, A. (2004). Occurrence of Bremia lactucae in natural populations of Lactuca serriola. Journal of Phytopathology, 152, 391–398.

    Article  Google Scholar 

  • Petrželová, I., Lebeda, A., Nevo, E., & Beharav, A. (2007). Variation of response against Bremia lactucae in natural populations of Lactuca saligna. In A. Lebeda, & P. T. N. Spencer-Phillips (Eds.) Advances in downy mildew research, vol. 3. Proceedings of the 2nd international downy mildews symposium (pp. 169–173). Olomouc and Kostelec na Hané, Czech Republic: Palacký University in Olomouc and JOLA.

    Google Scholar 

  • Petřivalský, M., Kočířová, J., Sedlářová, M., Piterková, J., Luhová, L., & Lebeda, A. (2007). On the role of nitric oxide in Bremia lactucae pathogenesis on Lactuca sativa. In A. Lebeda, & P. T. N. Spencer-Phillips (Eds.) Advances in downy mildew research, vol. 3. Proceedings of the 2nd international downy mildews symposium (pp. 175–184). Olomouc and Kostelec na Hané, Czech Republic: Palacký University in Olomouc and JOLA.

    Google Scholar 

  • Pink, D. A. C. (2002). Strategies using genes for non-durable disease resistance. Euphytica, 124, 227–236.

    Article  CAS  Google Scholar 

  • Portz, D., Koch, E., & Slusarenko, A. (2008). Effects of garlic (Allium sativum) juice containing allicin on Phytophthora infestans and on downy mildew of cucumber caused by Pseudoperonospora cubensis. European Journal of Plant Pathology (this issue).

  • Prokopová, J., Nauš, J., Špundová, M., & Sedlářová, M. (2007). The effect of meta-topolin on optical parameters of lettuce leaf discs infected by Bremia lactucae. In A. Lebeda, & P. T. N. Spencer-Phillips (Eds.) Advances in downy mildew research, vol. 3. Proceedings of the 2nd international downy mildews symposium (pp. 73–78). Olomouc and Kostelec na Hané, Czech Republic: Palacký University in Olomouc and JOLA.

    Google Scholar 

  • Rees, S., & Harborne, J. (1984). Flavonoids and other phenolics of Cichorium and related members of the Lactuceae (Compositae). Botanical Journal of the Linnean Society, 89, 313–319.

    Article  Google Scholar 

  • Restrepo, S., Myers, K. L., del Pozo, O., Martin, G. B., Hart, A. L., Buell, C. R., et al. (2005). Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Molecular Plant–Microbe Interactions, 18, 913–922.

    Article  PubMed  CAS  Google Scholar 

  • Reuveni, R., Shimoni, M., & Crute, I. R. (1991). An association between high peroxidase activity in lettuce (Lactuca sativa) and field resistance do downy mildew (Bremia lactucae). Journal of Phytopathology, 132, 312–318.

    Article  Google Scholar 

  • Robatzek, S. (2007). Vesicle trafficking in plant immune responses. Cellular Microbiology, 9, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Saltveita, M. E., Choia, Y. J., & Tomás-Barberán, F. A. (2005). Mono-carboxylic acids and their salts inhibit wound-induced phenolic accumulation in excised lettuce (Lactuca sativa) leaf tissue. Physiologia Plantarum, 125, 454–463.

    Google Scholar 

  • Sargent, J. A. (1976). Germination of spores of Bremia lactucae. Annals of Applied Biology, 84, 290–294.

    Article  Google Scholar 

  • Sargent, J. A., & Payne, H. L. (1974). Effect of temperature on germination, viability and fine structure of conidia of Bremia lactucae. Transactions of British Mycological Society, 63, 509–518.

    Article  Google Scholar 

  • Sargent, J. A., Tommerup, I. C., & Ingram, D. S. (1973). The penetration of a susceptible lettuce variety by the downy mildew fungus, Bremia lactucae Regel. Physiological Plant Pathology, 3, 231–239.

    Article  Google Scholar 

  • Scharte, J., Schön, H., & Weis, E. (2005). Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant, Cell and Environment, 28, 1421–1435.

    Article  CAS  Google Scholar 

  • Schnabel, G., Strittmatter, G., & Noga, G. (1998). Changes in photosynthetic electron transport in potato cultivars with different field resistance after infection with Phytophthora infestans. Journal of Phytopathology, 146, 205–210.

    Article  CAS  Google Scholar 

  • Sedlářová, M., Binarová, P., & Lebeda, A. (2001a). Changes in microtubular alignment in Lactuca spp. (Asteraceae) epidermal cells during early stages of infection by Bremia lactucae (Peronosporaceae). Phyton, 41, 21–34.

    Google Scholar 

  • Sedlářová, M., & Lebeda, A. (2001). Histochemical detection and role of phenolic compounds in defence response of Lactuca spp. to lettuce downy mildew (Bremia lactucae). Journal of Phytopathology, 149, 1–5.

    Article  Google Scholar 

  • Sedlářová, M., Lebeda, A., & Pink, D. A. C. (2001b). The early stages of interaction between effective and non-effective race-specific genes in Lactuca sativa, wild Lactuca spp. and Bremia lactucae (race NL16). Journal of Plant Diseases and Protection, 108, 477–489.

    Google Scholar 

  • Sedlářová, M., Luhová, L., Petřivalský, M., & Lebeda, A. (2007a). Localisation and metabolism of reactive oxygen species during Bremia lactucae pathogenesis in Lactuca sativa and wild Lactuca spp. Plant Physiology and Biochemistry, 45, 607–616.

    Article  PubMed  CAS  Google Scholar 

  • Sedlářová, M., Výtisková, M., Doležal, K., & Lebeda, A. (2007b). Pre-incubation with cytokinins delays chlorophyll degradation in Lactuca spp. tissues and reduces Bremia lactucae sporulation. In A. Lebeda, & P. T. N. Spencer-Phillips (Eds.) Advances in downy mildew research, vol. 3. Proceedings of the 2nd international downy mildews symposium (pp. 185–194). Olomouc and Kostelec na Hané, Czech Republic: Palacký University in Olomouc and JOLA.

    Google Scholar 

  • Skidmore, D. I., & Ingram, D. S. (1985). Conidial morphology and the specialization of Bremia lactucae Regel (Peronosporaceae) on hosts in the family Compositae. Botanical Journal of the Linnean Society, 91, 503–522.

    Article  Google Scholar 

  • Spencer-Phillips, P. T. N. (1997). Function of fungal haustoria in epiphytic and endophytic infections. Advances in Botanical Research, 24, 309–333.

    Article  Google Scholar 

  • Takemoto, D., & Hardham, A. R. (2004). The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiology, 136, 3864–3876.

    Article  PubMed  CAS  Google Scholar 

  • Takemoto, D., Jones, D. A., & Hardham, A. R. (2003). GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. The Plant Journal, 33, 775–792.

    Article  PubMed  CAS  Google Scholar 

  • Tang, X., Rolfe, S. A., & Scholes, J. D. (1996). The effect of Albugo candida (white blister rust) on the photosynthetic and carbohydrate metabolism of leaves of Arabidopsis thaliana. Plant, Cell and Environment, 19, 967–975.

    Article  CAS  Google Scholar 

  • Thines, M. (2007). Use of scanning electron microscopy in downy mildew systematics. In A. Lebeda, & P. T. N. Spencer-Phillips (Eds.) Advances in downy mildew research, vol. 3. Proceedings of the 2nd international downy mildews symposium (pp. 17–23). Olomouc and Kostelec na Hané, Czech Republic: Palacký University in Olomouc and JOLA.

    Google Scholar 

  • Thines, M., Göker, M., Spring, O., & Oberwinkler, F. (2006). A revision of Bremia graminicola. Mycological Research, 110, 646–656.

    Article  PubMed  Google Scholar 

  • Van Pelt-Heerschap, H., & Smit-Bakker, O. (1993). Cell-wall degrading enzymes synthesized by the obligate pathogen Bremia lactucae. In B. Fritig, & M. Legrand (Eds.) Mechanisms of plant defense responses (p. 82). Dordrecht: Kluwer.

    Google Scholar 

  • Vieira, B. S., & Barreto, R. W. (2006). First record of Bremia lactucae infecting Sonchus oleraceus and Sonchus asper in Brazil and its infectivity to lettuce. Journal of Phytopathology, 154, 84–87.

    Article  Google Scholar 

  • Voglmayr, H. (2008). Progress and challenge in systematics of downy mildews and white blister rusts: New insights from genes and morphology. European Journal of Plant Pathology (this issue).

  • Voglmayr, H., Riethmuller, A., Göker, M., Weiss, M., & Oberwinkler, F. (2004). Phylogenetic relationships of Plasmopara, Bremia and other genera of downy mildew pathogens with pyriform haustoria based on Bayesian analysis of partial LSU rDNA sequence data. Mycological Research, 108, 1011–1024.

    Article  PubMed  CAS  Google Scholar 

  • Walters, D., & McRoberts, N. (2006). Plants and biotrophs: A pivotal role for cytokinins. Trends in Plant Science, 11, 581–586.

    Article  PubMed  CAS  Google Scholar 

  • Wasteneys, G. O. (2004). Progress in understanding the role of microtubules in plant cells. Current Opinion in Plant Biology, 7, 651–660.

    Article  PubMed  CAS  Google Scholar 

  • Witsenboer, H., Vogel, J., & Michelmore, R. W. (1997). Identification, genetic localization, and allelic diversity of selectively amplified microsatellite polymorphic loci in lettuce and wild relatives (Lactuca spp.). Genome, 40, 923–936.

    Article  PubMed  CAS  Google Scholar 

  • Woods, A. M., Fagg, J., & Mansfield, J. W. (1988). Fungal development and irreversible membrane damage in cells of Lactuca sativa undergoing the hypersensitive reaction to the downy mildew fungus Bremia lactucae. Physiological and Molecular Plant Pathology, 32, 483–498.

    Article  Google Scholar 

  • Zinkernagel, V. (1985). Investigations on the susceptibility and resistance of head lettuce (Lactuca sativa) to downy mildew (Bremia lactucae). 2. Light and electron-microscopic examinations of the host–parasite interface. Journal of Phytopathology, 112, 238–258.

    Article  Google Scholar 

  • Zinkernagel, V. (1986). Investigations on the susceptibility of head lettuce (Lactuca sativa) to downy mildew (Bremia lactucae). 3. Activities of peroxidase, catalase and polyphenoloxidase. Journal of Phytopathology, 115, 257–266.

    Article  CAS  Google Scholar 

  • Zinkernagel, V., & Bartscherer, H. C. (1978). The host–parasite interface in Bremia lactucae with Lactuca sativa. In Book of Abstracts, 3rd International Congress of Plant Pathology (p. 112). München, Germany.

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Acknowledgements

The work was funded by grants from the Czech Ministry of Education (MSM 6198959215) and Grant Agency of the Czech Republic (GP 522/02/D011). The authors thank Dr. P.T.N. Spencer-Phillips (UWE, Bristol, UK) for critical reading of the first draft of the manuscript, participants at the 2nd International Downy Mildews Symposium (Olomouc, Czech Republic, 2007) for valuable discussions, and Olympus C&S (Prague) for supporting the arrangement and development of the Laboratory of Confocal Microscopy in the Department of Botany at Palacky University in Olomouc.

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  1. Faculty of Science, Department of Botany, Palacký University, Šlechtitelů 11, 783 71, Olomouc-Holice, Czech Republic

    Aleš Lebeda & Michaela Sedlářová

  2. Faculty of Science, Department of Biochemistry, Palacký University, Šlechtitelů 11, 783 71, Olomouc-Holice, Czech Republic

    Marek Petřivalský

  3. Faculty of Science, Department of Experimental Physics, Palacký University, Tř. Svobody 26, 771 46,, Olomouc, Czech Republic

    Jitka Prokopová

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  1. Aleš Lebeda
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  2. Michaela Sedlářová
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Correspondence to Aleš Lebeda.

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Lebeda, A., Sedlářová, M., Petřivalský, M. et al. Diversity of defence mechanisms in plant–oomycete interactions: a case study of Lactuca spp. and Bremia lactucae . Eur J Plant Pathol 122, 71–89 (2008). https://doi.org/10.1007/s10658-008-9292-3

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