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Uromyces appendiculatus Infection in BTH-Treated Bean Plants: Ultrastructural Details of a Lost Fight

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Abstract

The mechanisms of BTH [benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester]-induced resistance against bean rust caused by Uromyces appendiculatus have been explored in Phaseolus vulgaris by light and transmission electron microscopy, following the infection progression in plants challenged 7 days after treatment. While BTH did not affect uredospore germination and fungal penetration in the substomatal cavity, a first impairment to the colonization appeared evident about 48–96 h after inoculation, with alterations of infection hypha structure and reduction in mycelium expansion. No differences were found in this phase regarding the formation and ultrastructure of haustoria in untreated and BTH-treated plants, except for the deposition of electron-opaque material in the extrahaustorial matrix of the latter. A second and decisive impairment in fungal progression was observed at 7–10 days after inoculation when host cell penetrated, or in close contact with the fungal hyphae, were impregnated by phenolic compounds. The same was observed in fungal walls, particularly around haustoria, thus hampering the biotrophic habitus of the fungus and further mycelium spreading. This, in turn, prevented the evasion of fungal reproductive structures, the uredinia, and the appearance of visible symptoms. No particular ultrastructural alterations were observed in most of the penetrated cells, even at late stages of infection, indicating that BTH treatment does not induce host cells to respond with a hypersensitive reaction (HR). A parallel time course of the expression of phenylalanine ammonia lyase (PAL) gene, the key enzyme for the synthesis of phenylpropanoidic phytoalexins and many other phenolics, has shown that PAL mRNA is strongly and persistently transcripted in BTH-treated plants since the 6th h after treatment, though no apparent ultrastructural alterations were detectable up to some days after pathogen challenging. This indicates that BTH, at the employed concentration of 0.3 mM, directly activates the plant’s own defences, thus accounting for the observed full protection against bean rust.

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References

  1. Iriti M, Faoro F. Review of innate and specific immunity in plants and animals. Mycopathologia. 2007;164:57–64.

    Article  PubMed  Google Scholar 

  2. Király L, Barna B, Király Z. Plant resistance to pathogen infection: forms and mechanisms of innate and acquired resistance. J Phytopathol. 2007;155:385–96.

    Article  Google Scholar 

  3. Greenberg JT. Programmed cell death in plant-pathogen interactions. Annu Rev Plant Physiol Mol Biol. 1997;48:525–45.

    Article  CAS  Google Scholar 

  4. Király L, Király Z. To die or not to die—is cell death dispensable for resistance during the plant hypersensitive response? Acta Phytopathol Entomol Hung. 2006;41:11–21.

    Article  Google Scholar 

  5. Mauch-Mani B, Métraux J-P. Salicylic acid and systemic acquired resistance to pathogen attack. Ann Bot. 1998;82:535–40.

    Article  CAS  Google Scholar 

  6. Conrath U. Systemic acquired resistance. Plant Signal Behav. 2006;1:179–84.

    PubMed  Google Scholar 

  7. Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323–9.

    Article  CAS  PubMed  Google Scholar 

  8. Schreiber K, Desveaux D. Message in a bottle: chemical biology of induced resistance in plants. Plant Pathol J. 2008;24:245–68.

    CAS  Google Scholar 

  9. Gozzo F. Systemic acquired resistance in crop protection: from nature to a chemical approach. J Agric Food Chem. 2003;51:4487–503.

    Article  CAS  PubMed  Google Scholar 

  10. Friedrich L, Lawton K, Ruess W, Mesner P, Speker N, Gut Rella M, Meier B, Dincher S, Staub T, Uknes S, Métraux JP, Kessmann H, Ryals J. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 1996;10:61–70.

    Article  CAS  Google Scholar 

  11. Görlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell. 1996;8:629–43.

    Article  PubMed  Google Scholar 

  12. Wendehenne D, Durner J, Chen Z, Klessig F. Benzothiadiazole, an inducer of plant defences, inhibits catalase and ascorbate peroxidase. Phytochemistry. 1998;47:651–7.

    Article  CAS  Google Scholar 

  13. Kohler A, Schwindling S, Conrath U. Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding and infiltration of water into leaves requires the NPR1/NIM1 gene in arabidopsis. Plant Physiol. 2002;128:1046–56.

    Article  CAS  PubMed  Google Scholar 

  14. Iriti M, Faoro F. Benzothiadiazole (BTH) induces cell-death independent resistance in Phaseolus vulgaris against Uromyces appendiculatus. J Phytopath. 2003;151:171–80.

    Article  CAS  Google Scholar 

  15. Faoro F, Maffi D, Cantu D, Iriti M. Chemical-induced resistance against powdery mildew in barley: the effects of chitosan and benzothiadiazole. Biocontrol. 2008;53:387–401.

    Article  CAS  Google Scholar 

  16. Lindgren DT, Eskridge KM, Steadman JR, Schaaf DM. A model for dry bean yield loss due to rust. HortTechnol. 1995;5:35–7.

    Google Scholar 

  17. Coyne DP, Steadman JR, Godoy-Lutz G, Gilbertson R, Arnaud-Santana E, Beaver JS, Myers JR. Contributions of the bean/cowpea CRSP to management of bean diseases. Field Crop Res. 2003;82:155–68.

    Article  Google Scholar 

  18. Maheshwari R, Allen PJ, Hildebrandt AC. Physical and chemical factors controlling the development of the infection structures from urediospores germ tubes of rust fungi. Phytopathology. 1967;57:855–62.

    CAS  Google Scholar 

  19. Heat MC, Skalamera D. Cellular interaction between plants and biotrophic fungal parasites. In: Tommerup IC, Andrews JH. editors. Advanced in botanical research vol. 24. San Diego: Academic Press; 1997. p. 195–225.

  20. Latunda-Dada AO, Lucas JA. The plant defence activator acibenzolar-S-methyl primes cowpea [Vigna unguicolata (L.) Walp.] seedlings for rapid induction of resistance. Physiol Mol Plant Pathol. 2001;58:199–208.

    Article  Google Scholar 

  21. Buzi A, Chilosi G, Magro P. Induction of resistance in melon seedlings against soil-borne fungal pathogens by gaseous treatments with methyl jasmonate and ethylene. J Phytopatol. 1994;152:491–7.

    Article  Google Scholar 

  22. Boava LP, Kuhn OJ, Pascholati SF, di Piero RM, Furtado EL. Effect of acibenzolar-S-methyl and Saccharomyces cerevisiae on the activation of Eucalyptus defences against rust. Australas Plant Pathol. 2009;38:594–602.

    Article  CAS  Google Scholar 

  23. Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B. Priming: getting ready for battle. Mol Plant Microbe Interact. 2006;19:1062–71.

    Article  CAS  PubMed  Google Scholar 

  24. Keogh RC, Deverall BJ, Mcleod S. Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans Br Mycol Soc. 1980;74:329–33.

    Article  Google Scholar 

  25. O’Brien TP, Feder N, Mc Cully ME. Polychromatic staining of plant cell walls by toluidine blue. Protoplasma. 1964;59:367–73.

    Google Scholar 

  26. Eschrich W, Currier HB. Identification of callose by its diachrome and fluorochrome reactions. Stain Technol. 1964;39:303–7.

    CAS  Google Scholar 

  27. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. Ford N editor. NY: Cold Spring Harbor Laboratory Press; 1989.

  28. Wojtaszek P, Trethowan J, Bolwell P. Reconstitution in vitro of the components and conditions required for the oxidative cross-linking of extracellular proteins in French bean (Phaseolus vulgaris L). FEBS Lett. 1997;405:95–8.

    Article  CAS  PubMed  Google Scholar 

  29. Kauss H, Jeblick W. Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiol. 1995;108:1171–8.

    CAS  PubMed  Google Scholar 

  30. Katz VA, Thulke OU, Conrath U. A benzothiadiazole primes parsely cells for augmented elicitation of defence responses. Plant Physiol. 1998;117:1333–9.

    Article  CAS  PubMed  Google Scholar 

  31. Alvarez ME, Pennell RI, Meijer PJ, Ishikatwa A, Dixon RA, Lamb C. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell. 1998;92:773–84.

    Article  CAS  PubMed  Google Scholar 

  32. Lin TC, Ishizaka M, Ishii H. Acibenzolar-S-methyl-induced systemic resistance against anthracnose and powdery mildew diseases on cucumber plants without accumulation of phytoalexins. J Phytopathol. 2009;157:40–50.

    Article  CAS  Google Scholar 

  33. Goellner K, Conrath U. Priming: it’s all the world to induced disease resistance. Eur J Plant Pathol. 2008;121:233–42.

    Article  Google Scholar 

  34. McFadden HG, Chapple R, de Feyter R, Dennis E. Expression of pathogenesis related genes in cotton stems in response to infection by Verticillum dahaliae. Physiol Mol Plant Pathol. 2001;58:119–31.

    Article  CAS  Google Scholar 

  35. Cools HJ, Ishii H. Pre-treatment of cucumber plants with acibenzolar-S-methyl systemically primes a phenylalanine ammonia lyase gene (PAL1) for enhanced expression upon infection with a pathogenic fungus. Physiol Mol Plant Pathol. 2002;61:273–80.

    Article  CAS  Google Scholar 

  36. Whan JA, Dann EK, Smith LJ, Aitken EAB. Acybenzolar-S-methyl-induced alteration of defence gene expression and enzyme activity in cotton infected with Fusarium oxysporum f. sp. vasinfectum. Physiol Mol Plant Pathol. 2009;73:175–82.

    Article  Google Scholar 

  37. Walters DR, Fountaine JM. Practical application of induced resistance to plant diseases: an appraisal of effectiveness under field conditions. J Agric Sci. 2009;147:523–35.

    Article  CAS  Google Scholar 

  38. Iriti M, Faoro F. Does benzothiadiazole induced resistance increase fitness cost in bean? J Plant Pathol. 2003;85:265–70.

    CAS  Google Scholar 

  39. Nicholson RL, Hammerschmidt R. Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol. 1992;30:369–89.

    Article  CAS  Google Scholar 

  40. Benhamou N, Bélanger RR. Benzothiadiazole-mediated induced resistance to Fusarium oxysporum f. sp. radicis-lycopersici in tomato. Plant Physiol. 1998;118:1203–12.

    Article  CAS  PubMed  Google Scholar 

  41. Benhamou N, Bélanger RR. Induction of systemic resistance to Pythium damping-off in cucumber plants by benzothiadiazole: ultrastructure and cytochemistry of the host response. Plant J. 1998;14:13–21.

    Article  CAS  PubMed  Google Scholar 

  42. Scalet M, Crivaletto E, Mallardi F. Demonstration of phenolic compounds in plant tissues by an osmium-iodide postfixation procedure. Stain Technol. 1989;64:273–90.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This paper is dedicated to the memory of Dr. Massimo Pigni who suddenly died on 25th September 2009, soon after finishing his doctoral thesis of which this work is a fundamental part.

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Correspondence to Franco Faoro.

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D. Maffi and M. Iriti equally contributed to this work.

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Maffi, D., Iriti, M., Pigni, M. et al. Uromyces appendiculatus Infection in BTH-Treated Bean Plants: Ultrastructural Details of a Lost Fight. Mycopathologia 171, 209–221 (2011). https://doi.org/10.1007/s11046-010-9350-1

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