View More View Less
  • 1 Hungarian Academy of Sciences Plant Protection Institute, Centre for Agricultural Research H-1525 Budapest P.O.B. 102 Hungary
  • 2 Kafr-El-Sheikh University Department of Agricultural Botany, Plant Pathology Branch, Faculty of Agriculture 33516 Kafr-El-Sheikh Egypt
Restricted access

Purchase article

USD  $20.00

1 year subscription (Individual Only)

USD  $542.00

Similarities and differences in the immune systems of plants and animals are discussed in relation to non-specific and specific immunity (resistance), systemic acquired resistance (immune memory), transgenerational immune memory and gene silencing. Furthermore, we attempt to answer the question “what is inhibiting or killing pathogens during the immune (resistance) process”? Therefore, the possible roles of reactive oxygen species and antioxidants in pathogen inhibition are evaluated in different types of plant disease resistance.

  • Ádám, A., Farkas, T., Somlyai, G., Hevesi, M. and Király, Z. (1989): Consequence of O2− generation during a bacterially induced hypersensitive reaction in tobacco: deterioration of membrane lipids. Physiol. Molec. Plant Pathol. 34, 13–26.

    Király Z. , 'Consequence of O2− generation during a bacterially induced hypersensitive reaction in tobacco: deterioration of membrane lipids ' (1989 ) 34 Physiol. Molec. Plant Pathol : 13 -26.

    • Search Google Scholar
  • Akimoto, K., Katakami, H., Kim, H-J., Ogawa, E., Sano, C. M., Wada, Y. and Sano, H. (2007): Epigenetic inheritance in rice plants. Ann. Bot. 100, 205–217.

    Sano H. , 'Epigenetic inheritance in rice plants ' (2007 ) 100 Ann. Bot : 205 -217.

  • Alfano, J. R. and Collmer, A. (2004): Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42, 385–414.

    Collmer A. , 'Type III secretion system effector proteins: double agents in bacterial disease and plant defense ' (2004 ) 42 Annu. Rev. Phytopathol : 385 -414.

    • Search Google Scholar
  • Al-Mawaali, Q. S., Al-Sadi, A. M. and Deadman, M. K. (2013): Management of cucumber damping-off and vine decline by grafting on resistant rootstocks. Intern. Conf. Plant Diseases and Resistance Mechan. Vienna, Austria. Abstract, p. 76, N 80.

    Deadman M. K. , '', in Vienna, Austria. Abstract , (2013 ) -.

  • Alvarez, M. E., Nota, F. and Cambiagno, D. A. (2010): Epigenetic control of plant immunity. Mol. Plant Pathol. 11, 563–576.

    Cambiagno D. A. , 'Epigenetic control of plant immunity ' (2010 ) 11 Mol. Plant Pathol : 563 -576.

    • Search Google Scholar
  • Apel, K. and Hirt, H. (2004): Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399.

    Hirt H. , 'Reactive oxygen species: metabolism, oxidative stress, and signal transduction ' (2004 ) 55 Annu. Rev. Plant Biol : 373 -399.

    • Search Google Scholar
  • Ausubel, F. M. (2005): Are immune signaling pathways in plants and animals conserved? Nature Immunol. 6, 973–979.

    Ausubel F. M. , 'Are immune signaling pathways in plants and animals conserved? ' (2005 ) 6 Nature Immunol : 973 -979.

    • Search Google Scholar
  • Bacsó, R., Hafez, Y. M., Király, Z. and Király, L. (2011): Inhibition of virus replication and symptom expression by reactive oxygen species in tobacco infected with Tobacco mosaic virus. Acta Phytopathol. Entomol. Hung. 46, 1–10.

    Király L. , 'Inhibition of virus replication and symptom expression by reactive oxygen species in tobacco infected with Tobacco mosaic virus ' (2011 ) 46 Acta Phytopathol. Entomol. Hung : 1 -10.

    • Search Google Scholar
  • Baker, J. C. and Orlandi, E. W. (1995): Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299–321.

    Orlandi E. W. , 'Active oxygen in plant pathogenesis ' (1995 ) 33 Annu. Rev. Phytopathol : 299 -321.

    • Search Google Scholar
  • Balázs, E., Sziráki, I. and Király, Z. (1977): The role of cytokinins in systemic acquired resistance of tobacco hypersensitive to tobacco mosaic virus. Physiol. Plant Pathol. 11, 29–37.

    Király Z. , 'The role of cytokinins in systemic acquired resistance of tobacco hypersensitive to tobacco mosaic virus ' (1977 ) 11 Physiol. Plant Pathol : 29 -37.

    • Search Google Scholar
  • Bandaranayake, P. C. G. and Yoder, J. I. (2013): Trans-specific gene silencing of acetyl-coa carboxylase in a root-parasitic plant. Mol. Plant-Microbe Interactions 26, 575–584.

    Yoder J. I. , 'Trans-specific gene silencing of acetyl-coa carboxylase in a root-parasitic plant ' (2013 ) 26 Mol. Plant-Microbe Interactions : 575 -584.

    • Search Google Scholar
  • Barna, B., Ádám, A. and Király, Z. (1993): Juvenility and resistance of a superoxide-tolerant plant to diseases and other stresses. Naturwissenschaften 80, 420–422.

    Király Z. , 'Juvenility and resistance of a superoxide-tolerant plant to diseases and other stresses ' (1993 ) 80 Naturwissenschaften : 420 -422.

    • Search Google Scholar
  • Barna, B., Fodor, J., Harrach, B., Pogány, M. and Király, Z. (2012): The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol. Biochem. 59, 37–43.

    Király Z. , 'The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens ' (2012 ) 59 Plant Physiol. Biochem : 37 -43.

    • Search Google Scholar
  • Baulcombe, D. C. (1996): Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8, 1833–1844.

    Baulcombe D. C. , 'Mechanisms of pathogen-derived resistance to viruses in transgenic plants ' (1996 ) 8 Plant Cell : 1833 -1844.

    • Search Google Scholar
  • Baulcombe, D. (2004): RNA silencing in plants. Nature 431, 356–363.

    Baulcombe D. , 'RNA silencing in plants ' (2004 ) 431 Nature : 356 -363.

  • Bilichak, A., Ilnystkyy, Y., Hollunder, J. and Kovalchuk, I. (2012): The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS One 7, e30515.

    Kovalchuk I. , 'The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression ' (2012 ) 7 PLoS One : e30515 -.

    • Search Google Scholar
  • Boller, T. and Felix, G. A. (2009): A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379–406.

    Felix G. A. , 'A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors ' (2009 ) 60 Annu. Rev. Plant Biol : 379 -406.

    • Search Google Scholar
  • Boyko, A. and Kovalchuk, I. (2011): Genetic and epigenetic effects of plant–pathogen interactions: an evolutionary perspective. Mol. Plant 4, 1014–1023.

    Kovalchuk I. , 'Genetic and epigenetic effects of plant–pathogen interactions: an evolutionary perspective ' (2011 ) 4 Mol. Plant : 1014 -1023.

    • Search Google Scholar
  • Boyko, A., Kathiria, P., Zemp, F. J., Yao, Y., Pogribny, I. and Kovalchuk, I. (2007): Transgenerational changes in the genome stability and methylation in pathogen-infected plants (virus-induced plant genome instability). Nucleic Acids Res. 35, 1714–1725.

    Kovalchuk I. , 'Transgenerational changes in the genome stability and methylation in pathogen-infected plants (virus-induced plant genome instability) ' (2007 ) 35 Nucleic Acids Res : 1714 -1725.

    • Search Google Scholar
  • Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., Hollander, J., Meins, F. Jr. and Kovalchuk, I. (2010): Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS One 5, e9514.

    Kovalchuk I. , 'Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins ' (2010 ) 5 PLoS One : e9514 -.

    • Search Google Scholar
  • Carone, B. R., Fauquire, L., Habib, N., Shea, J. M. et al. (2010): Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084–1096.

    Shea J. M. , 'Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals ' (2010 ) 143 Cell : 1084 -1096.

    • Search Google Scholar
  • Carthew, R. W. (2001): Gene silencing by double-stranded RNA. Curr. Opin. Cell Biol. 13, 244–248.

    Carthew R. W. , 'Gene silencing by double-stranded RNA ' (2001 ) 13 Curr. Opin. Cell Biol : 244 -248.

    • Search Google Scholar
  • Chiriac, G. I., Andronic, L. I., Bujoreanu, V. V. and Marii, L. I. (2006): Features of crossing-over in virus-infected tomato. Centr. Eur. J. Biol. 1, 386–398.

    Marii L. I. , 'Features of crossing-over in virus-infected tomato ' (2006 ) 1 Centr. Eur. J. Biol : 386 -398.

    • Search Google Scholar
  • Chung, E. H., da Cunha, L., Wu, A. J., Gao, Z., Cherkis, K., Afzal, A. J., Mackey, D. and Dangl, J. L. (2011): Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9, 125–136.

    Dangl J. L. , 'Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants ' (2011 ) 9 Cell Host Microbe : 125 -136.

    • Search Google Scholar
  • Darkó, É., Ambrus, H., Szabó, I., Fodor, J., Király, Z. and Barnabás, B. (2009): Enhanced tolerance to oxidative stress with elevated antioxidant capacity in doubled haploid maize derived from microspores exposed to paraquat. Crop Sci. 49, 628–636.

    Barnabás B. , 'Enhanced tolerance to oxidative stress with elevated antioxidant capacity in doubled haploid maize derived from microspores exposed to paraquat ' (2009 ) 49 Crop Sci : 628 -636.

    • Search Google Scholar
  • Darkó, É., Fodor, J., Dulai, S., Ambrus, H., Szenzenstein, A., Király, Z. and Barnabás, B. (2011): Improved cold and drought tolerance of doubled haploid maize plants selected for resistance to prooxidant tert-butyl hydroperoxide. J. Agron. Crop Sci. 197, 454–465.

    Barnabás B. , 'Improved cold and drought tolerance of doubled haploid maize plants selected for resistance to prooxidant tert-butyl hydroperoxide ' (2011 ) 197 J. Agron. Crop Sci : 454 -465.

    • Search Google Scholar
  • Deák, M., Horváth, G. V., Davletova, S., Török, K., Sass, L., Vass, I., Barna, B., Király, Z. and Dudits, D. (1999): Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens. Nature Biotech. 17, 192–198.

    Dudits D. , 'Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens ' (1999 ) 17 Nature Biotech : 192 -198.

    • Search Google Scholar
  • Delledonne, M. (2005): NO news is good news for plants. Curr. Opin. Plant Biol. 8, 390–396.

    Delledonne M. , 'NO news is good news for plants ' (2005 ) 8 Curr. Opin. Plant Biol : 390 -396.

    • Search Google Scholar
  • Delledonne, M., Zeier, J., Marocco, A. and Lamb, C. (2001): Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA 98, 13454–13459.

    Lamb C. , 'Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response ' (2001 ) 98 Proc. Natl. Acad. Sci. USA : 13454 -13459.

    • Search Google Scholar
  • Dempsey, D. A. and Klessig, D. F. (2012): SOS — too many signals for systemic acquired resistance? Trends Plant Sci. 17, 538–545.

    Klessig D. F. , 'SOS — too many signals for systemic acquired resistance? ' (2012 ) 17 Trends Plant Sci : 538 -545.

    • Search Google Scholar
  • Doke, N. (1983): Involvement of a superoxide anion generation in the hypersensitive response of potato tube tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 23, 345–357.

    Doke N. , 'Involvement of a superoxide anion generation in the hypersensitive response of potato tube tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components ' (1983 ) 23 Physiol. Plant Pathol : 345 -357.

    • Search Google Scholar
  • Doke, N. and Ohashi, Y. (1988): Involvement of an O2 •− — generating system in the induction of necrotic lesions on tobacco leaves infected with Tobacco mosaic virus. Physiol. Molec. Plant Pathol. 32, 163–175.

    Ohashi Y. , 'Involvement of an O2•− — generating system in the induction of necrotic lesions on tobacco leaves infected with Tobacco mosaic virus ' (1988 ) 32 Physiol. Molec. Plant Pathol : 163 -175.

    • Search Google Scholar
  • Dong, X. (2004): Pathogen-induced systemic DNA rearrangement in plants. Trends Plant Sci. 9, 60–61.

    Dong X. , 'Pathogen-induced systemic DNA rearrangement in plants ' (2004 ) 9 Trends Plant Sci : 60 -61.

    • Search Google Scholar
  • Doss, M. M. (1981): Mechanism of systemic acquired resistance in cucumber caused by pathogenic and non-pathogenic agents. Ph.D. Diss. Res. Inst. Plant Protection, Budapest, 122 p.

    Doss M. M. , '', in Ph.D. Diss. Res. Inst. Plant Protection, Budapest , (1981 ) -.

  • Dowen, R. H., Pelizzola, M., Schmitza, R. J., Lister, R., Dowen, J. M., Nery, J. R., Dixon, J. E. and Ecker, J. R. (2012): Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl Acad. Sci. USA 109, E2183–E2191.

    Ecker J. R. , 'Widespread dynamic DNA methylation in response to biotic stress ' (2012 ) 109 Proc. Natl Acad. Sci. USA : E2183 -E2191.

    • Search Google Scholar
  • Dunoyer, P., Schott, G., Himber, C., Meyer, D., Takeda, A., Carrington, J. C. and Voinnet, O. (2010): Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912–916.

    Voinnet O. , 'Small RNA duplexes function as mobile silencing signals between plant cells ' (2010 ) 328 Science : 912 -916.

    • Search Google Scholar
  • Durrant, W. E. and Dong, X. (2004): Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209.

    Dong X. , 'Systemic acquired resistance ' (2004 ) 42 Annu. Rev. Phytopathol : 185 -209.

  • Eamens, A., Wang, M.-B., Smith, N. A. and Waterhouse, P. M. (2008): RNA silencing in plants: Yesterday, today, and tomorrow. Plant Physiol. 147, 456–468.

    Waterhouse P. M. , 'RNA silencing in plants: Yesterday, today, and tomorrow ' (2008 ) 147 Plant Physiol : 456 -468.

    • Search Google Scholar
  • El-Zahaby, H. M., Gullner, G. and Király, Z. (1995): Effects of powdery mildew infection of barley on the ascorbateglutathione cycle and other antioxidants in different host-pathogen interactions. Phytopathology 85, 1225–1230.

    Király Z. , 'Effects of powdery mildew infection of barley on the ascorbateglutathione cycle and other antioxidants in different host-pathogen interactions ' (1995 ) 85 Phytopathology : 1225 -1230.

    • Search Google Scholar
  • El-Zahaby, H. M., Hafez, Y. M. and Király, Z. (2004): Effect of reactive oxygen species on plant pathogens in planta and on disease symptoms. Acta Phytopathol. Entomol. Hung. 39, 325–345.

    Király Z. , 'Effect of reactive oxygen species on plant pathogens in planta and on disease symptoms ' (2004 ) 39 Acta Phytopathol. Entomol. Hung : 325 -345.

    • Search Google Scholar
  • Fabro, G., Steinbrenner, J., Coates, M., Ishaque, N., Baxter, L. et al. (2011): Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity. PLoS Pathog. 7, e1002348. doi:10.1371/journal.ppat.1002348.

    Baxter L. , 'Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity ' (2011 ) 7 PLoS Pathog : e1002348 -.

    • Search Google Scholar
  • Felix, G., Duran, J. D., Volko, S. and Boller, T. (1999): Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265–276.

    Boller T. , 'Plants have a sensitive perception system for the most conserved domain of bacterial flagellin ' (1999 ) 18 Plant J : 265 -276.

    • Search Google Scholar
  • Flor, H. H. (1971): Current status of the gene for gene concept. Annu. Rev. Phytopatol. 9, 275–296.

    Flor H. H. , 'Current status of the gene for gene concept ' (1971 ) 9 Annu. Rev. Phytopatol : 275 -296.

    • Search Google Scholar
  • Fodor, J., Gullner, G., Ádám, A. L., Barna, B., Kőmíves, T. and Király, Z. (1997): Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid. Plant Physiol. 114, 1443–1451.

    Király Z. , 'Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid ' (1997 ) 114 Plant Physiol : 1443 -1451.

    • Search Google Scholar
  • Forouhar, F., Yang, Y., Kumar, D., Chen, Y., Fridman, E., Park, S. W., Chiang, Y., Acton, T. B., Montelione, G. T., Pichersky, E., Klessig, D. F. and Tong, L. (2005): Crystal structure and biochemical studies identify tobacco SABP2 as a methylsalicylate esterase and further implicate it in plant innate immunity. Proc. Natl Acad. Sci. USA 102, 1773–1778.

    Tong L. , 'Crystal structure and biochemical studies identify tobacco SABP2 as a methylsalicylate esterase and further implicate it in plant innate immunity ' (2005 ) 102 Proc. Natl Acad. Sci. USA : 1773 -1778.

    • Search Google Scholar
  • Gassmann, W. and Bhattacharjee, S. (2012): Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. Mol. Plant-Microbe Interact. 25, 862–868.

    Bhattacharjee S. , 'Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks ' (2012 ) 25 Mol. Plant-Microbe Interact : 862 -868.

    • Search Google Scholar
  • Ghildiyal, M. and Zamore, P. (2009): Small silencing RNAs: An expanding universe. Nature Rev. Genet. 10, 94–108.

    Zamore P. , 'Small silencing RNAs: An expanding universe ' (2009 ) 10 Nature Rev. Genet : 94 -108.

    • Search Google Scholar
  • Goodman, R. N., Király, Z. and Wood, K. R. (1986): The biochemistry and physiology of plant disease. Univ. Missouri Press Columbia, MO.. 433 p.

    Wood K. R. , '', in The biochemistry and physiology of plant disease , (1986 ) -.

  • Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K. H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H. and Ryals, J. (1996): Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8, 629–643.

    Ryals J. , 'Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat ' (1996 ) 8 Plant Cell : 629 -643.

    • Search Google Scholar
  • Hafez, Y. M. and Király, Z. (2003): Role of hydrogen peroxide in symptom expression of barley susceptible and resistant to powdery mildew. Acta Phytopathol. Entomol. Hung. 38, 227–236.

    Király Z. , 'Role of hydrogen peroxide in symptom expression of barley susceptible and resistant to powdery mildew ' (2003 ) 38 Acta Phytopathol. Entomol. Hung : 227 -236.

    • Search Google Scholar
  • Hafez, Y. M., Fodor, J. and Király, Z. (2004): Establishment of acquired resistance confers reduced levels of superoxide and hydrogen-peroxide in TMV-infected tobacco leaves. Acta Phytopathol. Entomol. Hung. 39, 347–359.

    Király Z. , 'Establishment of acquired resistance confers reduced levels of superoxide and hydrogen-peroxide in TMV-infected tobacco leaves ' (2004 ) 39 Acta Phytopathol. Entomol. Hung : 347 -359.

    • Search Google Scholar
  • Hafez, Y. M., Király, Z. and Manninger, K. (2009): Hydrogen peroxide has a key role in resistance to leaf rust (Puccinia triticina) in several Egyptian and other wheat cultivars. Cereal Res. Commun. Suppl. 37, 161–164.

    Manninger K. , 'Hydrogen peroxide has a key role in resistance to leaf rust (Puccinia triticina) in several Egyptian and other wheat cultivars ' (2009 ) 37 Cereal Res. Commun. Suppl : 161 -164.

    • Search Google Scholar
  • Hafez, Y. M., Bacsó, R., Király, Z., Künstler, A. and Király, L. (2012): Up-regulation of antioxidants in tobacco by low concentrations of H2O2 suppresses necrotic disease symptoms. Phytopathology 102, 848–856.

    Király L. , 'Up-regulation of antioxidants in tobacco by low concentrations of H2O2 suppresses necrotic disease symptoms ' (2012 ) 102 Phytopathology : 848 -856.

    • Search Google Scholar
  • Halliwell, B. and Gutteridge, J. M. C. (1999): Free Radicals in Biology and Medicine. Oxford University Press, Inc. New York.

    Gutteridge J. M. C. , '', in Free Radicals in Biology and Medicine , (1999 ) -.

  • Hamilton, A. J., Brown, S., Yuanhai, H., Ishiuka, M., Lowe, A., Alpuche Solis, A.-G. and Grierson, D. (1998): A transgene with repeated DNA causes high frequency, post-transcriptional suppression of ACC-oxidase gene expression in tomato. Plant J. 15, 737–746.

    Grierson D. , 'A transgene with repeated DNA causes high frequency, post-transcriptional suppression of ACC-oxidase gene expression in tomato ' (1998 ) 15 Plant J : 737 -746.

    • Search Google Scholar
  • Hammerschmidt, R., Nuckles, E. M. and Kuc, J. (1982): Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol. Plant Pathol. 20, 73–82.

    Kuc J. , 'Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium ' (1982 ) 20 Physiol. Plant Pathol : 73 -82.

    • Search Google Scholar
  • Harrach, B. D., Fodor, J., Pogány, M., Preuss, J. and Barna, B. (2008): Antioxidant, ethylene and membrane leakage responses to powdery mildew infection of near-isogenic barley lines with various types of resistance. Eur. J. Plant Pathol. 121, 21–33.

    Barna B. , 'Antioxidant, ethylene and membrane leakage responses to powdery mildew infection of near-isogenic barley lines with various types of resistance ' (2008 ) 121 Eur. J. Plant Pathol : 21 -33.

    • Search Google Scholar
  • Harrach, B. D., Baltruschat, H., Barna, B., Fodor, J. and Kogel, K. H. (2013): The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol. Plant-Microbe Interact. 26, 599–605.

    Kogel K. H. , 'The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum ' (2013 ) 26 Mol. Plant-Microbe Interact : 599 -605.

    • Search Google Scholar
  • Jaskiewicz, M., Conrath, U. and Peterhänsel, C. (2011): Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12, 50–55.

    Peterhänsel C. , 'Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response ' (2011 ) 12 EMBO Rep : 50 -55.

    • Search Google Scholar
  • Jones, A. M. and Dangl, J. L. (2006): The plant immune system. Nature 444, 323–329.

    Dangl J. L. , 'The plant immune system ' (2006 ) 444 Nature : 323 -329.

  • Kale, S. D., Gu, B., Capelluto, D. G., Dou, D. et al. (2010): External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142, 284–295.

    Dou D. , 'External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells ' (2010 ) 142 Cell : 284 -295.

    • Search Google Scholar
  • Király, L., Hafez, Y. M., Fodor, J. and Király, Z. (2008): Suppression of tobacco mosaic virus-induced hypersensitivetype necrotisation in tobacco at high temperature is associated with down-regulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J. Gen. Virol. 89, 799–808.

    Király Z. , 'Suppression of tobacco mosaic virus-induced hypersensitivetype necrotisation in tobacco at high temperature is associated with down-regulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase ' (2008 ) 89 J. Gen. Virol : 799 -808.

    • Search Google Scholar
  • Király, L., Künstler, A., Hafez, Y. M., Király, Z. and Bacsó, R. (2013): Heat-induced susceptibility of barley to a biotrophic and a hemibiotrophic pathogen — differential changes in superoxide levels. 11th International Conference on Reactive Oxygen and Nitrogen Species in Plants, Warsaw, Poland. Abstract, BioTechnol. 94, 179.

    Bacsó R. , 'Heat-induced susceptibility of barley to a biotrophic and a hemibiotrophic pathogen — differential changes in superoxide levels. 11th International Conference on Reactive Oxygen and Nitrogen Species in Plants, Warsaw, Poland ' (2013 ) 94 Abstract, BioTechnol : 179 -.

    • Search Google Scholar
  • Király, Z., Barna, B. and Érsek, T. (1972): Hypersensitivity as a consequence, not the cause, of plant disease resistance to infection. Nature 239, 215–219.

    Érsek T. , 'Hypersensitivity as a consequence, not the cause, of plant disease resistance to infection ' (1972 ) 239 Nature : 215 -219.

    • Search Google Scholar
  • Király, Z., Barna, B., Kecskés, A. and Fodor, J. (2002): Down-regulation of antioxidative capacity in a transgenic tobacco which fails to develop acquired resistance to necrotization caused by tobacco mosaic virus. Free Rad. Res. 36, 981–991.

    Fodor J. , 'Down-regulation of antioxidative capacity in a transgenic tobacco which fails to develop acquired resistance to necrotization caused by tobacco mosaic virus ' (2002 ) 36 Free Rad. Res : 981 -991.

    • Search Google Scholar
  • Kogel, K.-H., Beckhove, U., Dreschers, J., Munch, S. and Romme, Y. (1994): Acquired resistance in barley. The resistance mechanism induced by 2,6-dichloroisonicotinic acid is a phenocopy of a genetically based mechanism governing race-specific powdery mildew resistance. Plant Physiol. 106, 1269–1277.

    Romme Y. , 'Acquired resistance in barley. The resistance mechanism induced by 2,6-dichloroisonicotinic acid is a phenocopy of a genetically based mechanism governing race-specific powdery mildew resistance ' (1994 ) 106 Plant Physiol : 1269 -1277.

    • Search Google Scholar
  • Kovalchuk, I., Kovalchuk, O., Kalck, V., Boyko, V., Filkowski, J., Heinlein, M. and Hohn, B. (2003): Pathogeninduced systemic plant signal triggers DNA rearrangements. Nature 423, 760–762.

    Hohn B. , 'Pathogeninduced systemic plant signal triggers DNA rearrangements ' (2003 ) 423 Nature : 760 -762.

    • Search Google Scholar
  • Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. (1994): H2O2 from the oxidative burst orchestrated the plant hypersensitive disease resistance response. Cell 79, 583–593.

    Lamb C. , 'H2O2 from the oxidative burst orchestrated the plant hypersensitive disease resistance response ' (1994 ) 79 Cell : 583 -593.

    • Search Google Scholar
  • Liu, P-P., Bhattacharjee, S., Klessig, D. F. and Moffett, P. (2010): Systemic acquired resistance is induced by Rgene-mediated responses independent of cell death. Molec. Plant Pathol. 11, 155–160.

    Moffett P. , 'Systemic acquired resistance is induced by Rgene-mediated responses independent of cell death ' (2010 ) 11 Molec. Plant Pathol : 155 -160.

    • Search Google Scholar
  • Liu, J., Elmore, J. M., Lin, Z. J. D. and Coaker, G. (2011): A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9, 137–146.

    Coaker G. , 'A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor ' (2011 ) 9 Cell Host Microbe : 137 -146.

    • Search Google Scholar
  • Luna, E., Bruce, T. J., Roberts, M. R., Flors, V. and Ton, J. (2012): Next generation systemic acquired resistance. Plant Physiol. 158, 844–853.

    Ton J. , 'Next generation systemic acquired resistance ' (2012 ) 158 Plant Physiol : 844 -853.

    • Search Google Scholar
  • Maekawa, T., Kufer, T. A. and Schulze-Lefert, P. (2011): NLR functions in plant and animal immune systems: so far and yet so close. Nature Immunol. 12, 818–826.

    Schulze-Lefert P. , 'NLR functions in plant and animal immune systems: so far and yet so close ' (2011 ) 12 Nature Immunol : 818 -826.

    • Search Google Scholar
  • Malamy, J., Carr, J. P., Classig, D. F. and Raskin, I. (1990): A likely endogenous signal in the resistance response of tobacco to viral infection. Science, 250, 1002–1004.

    Raskin I. , 'A likely endogenous signal in the resistance response of tobacco to viral infection ' (1990 ) 250 Science : 1002 -1004.

    • Search Google Scholar
  • Marino, D., Dunand, C., Puppo, A. and Pauly, N. (2012): A burst of plant NADPH oxidases. Trends Plant Sci. 17, 9–15.

    Pauly N. , 'A burst of plant NADPH oxidases ' (2012 ) 17 Trends Plant Sci : 9 -15.

  • Matzinger, P. (2002): The danger model: A renewed sense of self. Science 296, 301–305.

    Matzinger P. , 'The danger model: A renewed sense of self ' (2002 ) 296 Science : 301 -305.

  • Métraux, J-P., Singer, H., Rials, J. et al. (1990): Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004–1006.

    Rials J. , 'Increase in salicylic acid at the onset of systemic acquired resistance in cucumber ' (1990 ) 250 Science : 1004 -1006.

    • Search Google Scholar
  • Molinier, J., Ries, G., Zipfel, C. and Hohn, B. (2006): Transgeneration memory of stress in plants. Nature 442, 1046–1049.

    Hohn B. , 'Transgeneration memory of stress in plants ' (2006 ) 442 Nature : 1046 -1049.

  • Molnar, A., Melnyk, C. W., Bassett, A., Hardcastle, T. J., Dunn, R. and Baulcombe, D. C. (2010): Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872–875.

    Baulcombe D. C. , 'Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells ' (2010 ) 328 Science : 872 -875.

    • Search Google Scholar
  • Morel, F., Doussiere, J. and Vignais, P. V. (1991): The superoxide-generating oxidase of phagocytic cells. Physiological, molecular and pathological aspects. Eur. J. Biochem. 201, 523–546.

    Vignais P. V. , 'The superoxide-generating oxidase of phagocytic cells. Physiological, molecular and pathological aspects ' (1991 ) 201 Eur. J. Biochem : 523 -546.

    • Search Google Scholar
  • Mou, Z., Fan, W. and Dong, X. (2003): Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935–944.

    Dong X. , 'Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes ' (2003 ) 113 Cell : 935 -944.

    • Search Google Scholar
  • Mukhtar, M. S., Carvunis, A. R., Dreze, M. N., Epple, P. et. al. (2011): Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596–601.

    Epple P. , 'Independently evolved virulence effectors converge onto hubs in a plant immune system network ' (2011 ) 333 Science : 596 -601.

    • Search Google Scholar
  • Napoli, C., Lemieux, C. and Jorgensen, R. (1990): Introduction of a chimeric chalcone synthase gene into Petunia results in reversible cosuppression of homologous genes in trans. Plant Cell 2, 279–289.

    Jorgensen R. , 'Introduction of a chimeric chalcone synthase gene into Petunia results in reversible cosuppression of homologous genes in trans ' (1990 ) 2 Plant Cell : 279 -289.

    • Search Google Scholar
  • Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T. and Jones, J. D. G. (2004): The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113–1128.

    Jones J. D. G. , 'The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis ' (2004 ) 135 Plant Physiol : 1113 -1128.

    • Search Google Scholar
  • Netea, M. G., Quintin, J. and van der Meer, J. W. (2011): Trained immunity: A memory for innate host defense. Cell Host Microbe 9, 355–361.

    Meer J. W. , 'Trained immunity: A memory for innate host defense ' (2011 ) 9 Cell Host Microbe : 355 -361.

    • Search Google Scholar
  • Park, S-W., Kaimoyo, E., Kumar, D., Mosher, S. and Klessig, D. F. (2007): Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113–116.

    Klessig D. F. , 'Methyl salicylate is a critical mobile signal for plant systemic acquired resistance ' (2007 ) 318 Science : 113 -116.

    • Search Google Scholar
  • Pogány, M., von Rad, U., Grün, S., Dongó, A., Pintye, A., Simoneau, P., Bahnweg, G., Kiss, L., Barna, B. and Durner, J. (2009): Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol. 151, 1459–1475.

    Durner J. , 'Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem ' (2009 ) 151 Plant Physiol : 1459 -1475.

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

    Hückelhoven R. , 'RBOHF2 of barley is required for normal development of penetration resistance to the parasitic fungus Blumeria graminis f. sp. hordei ' (2010 ) 23 Molec. Plant-Microbe Interact : 1143 -1150.

    • Search Google Scholar
  • Rast, J. P., Smith, L. C., Loza-Coll, M., Hibino, T. and Litman, G. W. (2006): Genomic insights into the immune system of the sea urchin. Science 314, 952–956.

    Litman G. W. , 'Genomic insights into the immune system of the sea urchin ' (2006 ) 314 Science : 952 -956.

    • Search Google Scholar
  • Ronald, P. C. and Beutler, B. (2010): Plant and animal sensors of conserved microbial signatures. Science 330, 1061–1064.

    Beutler B. , 'Plant and animal sensors of conserved microbial signatures ' (2010 ) 330 Science : 1061 -1064.

    • Search Google Scholar
  • Ross, A. F. (1961): Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340–358.

    Ross A. F. , 'Systemic acquired resistance induced by localized virus infections in plants ' (1961 ) 14 Virology : 340 -358.

    • Search Google Scholar
  • Ruiz-Ferrer, V. and Voinnet, O. (2009): Role of plant small RNAs in biotic stress responses. Annu. Rev. PlantBiol. 60, 485–510.

    Voinnet O. , 'Role of plant small RNAs in biotic stress responses ' (2009 ) 60 Annu. Rev. PlantBiol : 485 -510.

    • Search Google Scholar
  • Samuel, G. (1931): Some experiments on inoculating methods with plant viruses and on local lesions. Ann. Appl. Biol. 18, 494–507.

    Samuel G. , 'Some experiments on inoculating methods with plant viruses and on local lesions ' (1931 ) 18 Ann. Appl. Biol : 494 -507.

    • Search Google Scholar
  • Schulze-Lefert, P. and Bieri, S. (2005): Recognition at a distance. Science 308, 506–508.

    Bieri S. , 'Recognition at a distance ' (2005 ) 308 Science : 506 -508.

  • Shah, J. and Zeier, J. (2013): Long-distance communication and signal amplification in systemic acquired resistance. Frontiers Plant Sci. 4, Art. 30.

    Zeier J. , 'Long-distance communication and signal amplification in systemic acquired resistance ' (2013 ) 4 Frontiers Plant Sci : 30 -.

    • Search Google Scholar
  • Shang, J., Xi, D.-H., Yuan, S. et al. (2010): Difference of physiological characters in dark green islands and yellow leaf tissue of Cucumber mosaic virus (CMV)-infected Nicotiana tabacum leaves. Z. Naturforsch. 65c, 73–78.

    Yuan S. , 'Difference of physiological characters in dark green islands and yellow leaf tissue of Cucumber mosaic virus (CMV)-infected Nicotiana tabacum leaves ' (2010 ) 65c Z. Naturforsch : 73 -78.

    • Search Google Scholar
  • Silhavy, D. and Burgyán, J. (2004): Effects and side-effects of viral RNA silencing suppressors on short RNAs. Trends Plant Sci. 9, 57–104.

    Burgyán J. , 'Effects and side-effects of viral RNA silencing suppressors on short RNAs ' (2004 ) 9 Trends Plant Sci : 57 -104.

    • Search Google Scholar
  • Spoel, S. H. and Dong, X. (2012): How do plants achieve immunity? Defence without specialized immune cells. Nature Rev. Immunol. 12, 89–100.

    Dong X. , 'How do plants achieve immunity? Defence without specialized immune cells ' (2012 ) 12 Nature Rev. Immunol : 89 -100.

    • Search Google Scholar
  • Staskawicz, B. J., Ausubel, F. F., Baker, B. J., Ellis, J. G. and Jones, J. D. G. (1995): Molecular genetics of plant disease resistance. Science 268, 661–667.

    Jones J. D. G. , 'Molecular genetics of plant disease resistance ' (1995 ) 268 Science : 661 -667.

    • Search Google Scholar
  • Strobel, N. E., and Kuc, J. (1995): Chemical and biological inducers of systemic resistance to pathogens protect cucumber and tobacco plants from damage caused by paraquat and cupric chloride. Phytopathology 85, 1306–1310.

    Kuc J. , 'Chemical and biological inducers of systemic resistance to pathogens protect cucumber and tobacco plants from damage caused by paraquat and cupric chloride ' (1995 ) 85 Phytopathology : 1306 -1310.

    • Search Google Scholar
  • Šutic, D. (1965): Vegetative effect of some plants on the curing of plum infected with Sharka (Plum Pox) virus. Zaštita bilja 88, 347–351.

    Šutic D. , 'Vegetative effect of some plants on the curing of plum infected with Sharka (Plum Pox) virus ' (1965 ) 88 Zaštita bilja : 347 -351.

    • Search Google Scholar
  • Sziráki, I., Balázs, E. and Király, Z. (1980): Role of different stresses in inducing systemic acquired resistance to TMV and increasing cytokinin level in tobacco. Physiol. Plant Pathol. 16, 277–284.

    Király Z. , 'Role of different stresses in inducing systemic acquired resistance to TMV and increasing cytokinin level in tobacco ' (1980 ) 16 Physiol. Plant Pathol : 277 -284.

    • Search Google Scholar
  • Szittya, Gy., Molnár, A., Silhavy, D., Hornyik, Cs. and Burgyán, J. (2002): Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell 14, 359–372.

    Burgyán J. , 'Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus ' (2002 ) 14 Plant Cell : 359 -372.

    • Search Google Scholar
  • Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H-S., Han, B., Zhu, T., Zou, G. and Katagiri, F. (2003): Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15, 317–330.

    Katagiri F. , 'Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae ' (2003 ) 15 Plant Cell : 317 -330.

    • Search Google Scholar
  • Torres, M. A. and Dangl, J. L. (2005): Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397–403.

    Dangl J. L. , 'Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development ' (2005 ) 8 Curr. Opin. Plant Biol : 397 -403.

    • Search Google Scholar
  • Torres, M. A., Jones, J. D. G. and Dangl, J. L. (2006): Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373–378.

    Dangl J. L. , 'Reactive oxygen species signaling in response to pathogens ' (2006 ) 141 Plant Physiol : 373 -378.

    • Search Google Scholar
  • van der Krol, A. R., Mur, L. A., Beld, M., Mol, J. and Stuitje, A. R. (1990): Flavonoid genes in petunia: Addition of a limited number of copies may lead to a suppression of gene expression. Plant Cell 2, 291–299.

    Stuitje A. R. , 'Flavonoid genes in petunia: Addition of a limited number of copies may lead to a suppression of gene expression ' (1990 ) 2 Plant Cell : 291 -299.

    • Search Google Scholar
  • Voinnet, O. (2001): RNA silencing as a plant immune system against viruses. Trends Genet. 17, 449–459.

    Voinnet O. , 'RNA silencing as a plant immune system against viruses ' (2001 ) 17 Trends Genet : 449 -459.

    • Search Google Scholar
  • Voinnet, O. (2005): Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Gen. 6, 206–220.

    Voinnet O. , 'Induction and suppression of RNA silencing: insights from viral infections ' (2005 ) 6 Nat. Rev. Gen : 206 -220.

    • Search Google Scholar
  • Vulic, T., Oparnica, C., Djordjević, B., Kuzmanović, S., Starović, M., Ford, E. and Tošić, M. (2013): Plum sectorial resistance to Plum pox virus is graft transmissible. Acta Phytopathol. Entomol. Hung. 48, 219–226.

    Tošić M. , 'Plum sectorial resistance to Plum pox virus is graft transmissible ' (2013 ) 48 Acta Phytopathol. Entomol. Hung : 219 -226.

    • Search Google Scholar
  • Waller, F., Achatz, B., Baltruschat, H., Fodor, J. et al. (2005): The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl Acad. Sci. USA 102, 13386–13391.

    Fodor J. , 'The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield ' (2005 ) 102 Proc. Natl Acad. Sci. USA : 13386 -13391.

    • Search Google Scholar
  • Wang, M-B., Masuta, C., Smith, N. A. and Shimura, H. (2012): RNA silencing and plant viral diseases. Mol. Plant-Microbe Interact. 25, 1275–1285.

    Shimura H. , 'RNA silencing and plant viral diseases ' (2012 ) 25 Mol. Plant-Microbe Interact : 1275 -1285.

    • Search Google Scholar
  • Ward, H. M. (1902): On the relations between host and parasite in the bromes and their brown rust, Puccinia dispersa (Erikss.). Ann. Bot. 16, 233–315.

    Ward H. M. , 'On the relations between host and parasite in the bromes and their brown rust, Puccinia dispersa (Erikss.) ' (1902 ) 16 Ann. Bot : 233 -315.

    • Search Google Scholar
  • Waterhouse, P. M., Graham, H. W. and Wang, M. B. (1998): Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc. Natl Acad. Sci. USA 95, 13959–13964.

    Wang M. B. , 'Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA ' (1998 ) 95 Proc. Natl Acad. Sci. USA : 13959 -13964.

    • Search Google Scholar
  • White, R. F. (1979): Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99, 410–412.

    White R. F. , 'Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco ' (1979 ) 99 Virology : 410 -412.

    • Search Google Scholar
  • Zipfel, C. and Rathjen, J. P. (2008): Plant immunity: AvrPto targets the frontline. Curr. Biol. 18, R218–R220.

    Rathjen J. P. , 'Plant immunity: AvrPto targets the frontline ' (2008 ) 18 Curr. Biol : R218 -R220.

    • Search Google Scholar
  • Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D. G., Felix, G. and Boller, T. (2004): Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767.

    Boller T. , 'Bacterial disease resistance in Arabidopsis through flagellin perception ' (2004 ) 428 Nature : 764 -767.

    • Search Google Scholar