Skip to main content
Log in

Chemical-induced resistance against powdery mildew in barley: the effects of chitosan and benzothiadiazole

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Chitosan (CHT), a deacetylated chitin derivative, and benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH), a non toxic synthetic functional analogue of salicylic acid, were applied as foliar spray to barley plants (Hordeum vulgare L.), to compare their effectiveness in inducing resistance against Blumeria graminis f. sp. hordei and to investigate the underlying defence response. After an induction phase of 3 days (IP, time elapsed between treatment and fungal inoculation) both compounds reduced significantly the infection on the primary leaf, namely of 55.5% for CHT and of 68.9% for BTH, showing the induction of a good level of local resistance (LAR). A 5-day IP further reduced the infected areas in BTH treated plants (−77.2%) but not in CHT treated ones (−47.1%). Furthermore, both CHT and BTH also induced SAR, being the infection in the second non treated leaves reduced of 57% and 76.2%, respectively, as evaluated at 10-day IP. Both BTH and CHT induced oxidative burst and phenolic compound deposition in treated leaves, creating an hostile environment that slowed down the fungal spreading by impairing haustorium development. However, the greater efficacy of BTH was possibly due to: i) a greater reinforcement of papilla; ii) a higher level and the more homogeneous diffusion of H2O2 in the treated leaf tissues and iii) an induced hypersensitive-like response in many penetrated cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aist JR, Bushnell WR (1981) Invasion of plant host by powdery mildew fungi and cellular mechanism of resistance. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 321–345

    Google Scholar 

  • Aist JR, Israel HW (1986) Autofluorescent and ultraviolet-absorbing components in cell wall and papillae of barley coleoptiles and their relationship to disease resistance. Can J Bot 64:266–272

    Article  Google Scholar 

  • Benhamou N, Theriault G (1992) Treatment with CHT enhances resistance of tomato plants to the crown and root rot pathogen Fusarium oxysporium f. sp. radicis-lycopersici. Physiol Mol Plant Path 41:33–52

    Article  CAS  Google Scholar 

  • Ben-Shalom N, Fallik E (2003) Further suppression of Botrytis cinerea disease in cucumber seedlings by chitosan-copper complex as compared with chitosan alone. Phytoparasitica 31:99–102

    CAS  Google Scholar 

  • Beßer K, Jarosch B, Langen G, Kogel KH (2000) Expression analysis of genes induced in barley after chemical activation reveals distinct disease resistance pathways. Mol Plant Pathol 1:277–286

    Article  Google Scholar 

  • Bradford M (1976) A rapid sensitive method for the quantisation of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Brugnerotto J, Desbrieres J, Roberts G, Rinaudo M (2001) Characterization of chitosan by steric exclusion chromatography. Polymer 42:9921–9927

    Article  CAS  Google Scholar 

  • Carver TLW, Jones SW (1988) Colony development by Erysiphe graminis f.sp. hordei on isolated epidermis of barley coleoptile incubated under continuous light or short-day conditions. Trans Br Mycol Soc 90:114–117

    Google Scholar 

  • Carver TLW, Zeyen RJ, Lyngkjaer MF (1995) Plant cell defences to powdery mildew of Gramineae. In: Walters DR, Scholes JD, Bryson RJ, Paul ND, Mc Roberts N (eds) Physiological responses of plants to pathogens. Aspects of applied biology, vol 42. Association of Applied Biologists, Warwick, pp 257–266

    Google Scholar 

  • Carver TLW, Ingerson-Morris SM, Thomas BJ (1996) Influences of host surface features on development of Erysiphe graminis and Erysiphe pisi. In: Kerstiens G (ed) Plant cuticles—an integrated functional approach. Bios Scientific Pub, Oxford, pp 255–266

    Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886

    Article  PubMed  CAS  Google Scholar 

  • Chen H-P, Xu L-L (2005) Isolation and characterization of a novel chitosan-binding protein from non-heading chinese cabbage leaves. J Integr Plant Biol 47:452–456

    Article  CAS  Google Scholar 

  • Doares H, Syrovets T, Weiler EW, Ryan CA (1995) Oligolacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci USA 92:4095–4098

    Article  PubMed  CAS  Google Scholar 

  • Du H, Klessig DF (1997) Identification of a soluble, high-affinity salicylic acid binding protein in tobacco. Plant Physiol 113:1319–1327

    PubMed  CAS  Google Scholar 

  • El-Ghaouth A, Arul J, Asselin A (1992) Antifungal activity of chitosan on two pathogens of strawberry fruits. Phytopathology 82:398–402

    Article  CAS  Google Scholar 

  • El-Zahaby HM, Gullner G, Kiraly Z (1995) Effects of powdery mildew infection of barley on the ascorbate-glutathione cycle and other antioxidants in different host-pathogen interactions. Phytopathology 85:1225–1230

    Article  CAS  Google Scholar 

  • Ellingboe AH (1972) Genetics and physiology of primary infection by Erysiphe graminis. Phytopathology 62:401–406

    Article  Google Scholar 

  • Eschrich W, Currier HB (1964) Identification of callose by its diachrome and fluorochrome reactions. Stain Technol 39:303–307

    CAS  Google Scholar 

  • Faoro F, Sant S, Iriti M, Appiano A (2001) Chitosan-elicited resitance to plant viruses: a histochemical and cytochemical study. In: Muzzarelli RAA (ed) Chitin enzymology. Atec, Italy, pp 57–62

    Google Scholar 

  • Faoro F, Iriti M (2005) Cell death or not cell death: two different mechanisms for chitosan and BTH antiviral activity. IOBC/WPRS Bull 29(8):25–29

    Google Scholar 

  • Friedrich L, Lawton K, Ruess W, Mesner P, Speker N, Gutrella M, Meier B, Dincher S, Staub T, Uknes S, Metraux JP, Kessmann H, Ryals J (1996) A benzothiadazole derivative induces systemic acquired resistance in tobacco. Plant J 10:61–70

    Article  CAS  Google Scholar 

  • Görlach J, Volrath S, Knauf-Beiter 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. Plant Cell 8:629–643

    Article  PubMed  Google Scholar 

  • Gozzo F (2003) Systemic acquired resistance in crop protection: from nature to a chemical approach. J Agric Food Chem 51:4487–4503

    Article  PubMed  CAS  Google Scholar 

  • Hadwiger LA, Beckman JM (1980) Chitosan as a component of Pea-Fusarium solani interaction. Plant Physiol 66:205–211

    Article  PubMed  CAS  Google Scholar 

  • Hadwiger LA, Ogawa OT, Kuyama H (1994) Chitosan polymer sizes effective in inducing phytoalexin accumulation and fungal suppression are verified with synthesized oligomers. Mol Plant–Microbe Interact 7:531–533

    PubMed  CAS  Google Scholar 

  • Heath MC (1998) Apoptosis, programmed cell death and the hypersensitive response. Eur J Plant Pathol 104:117–124

    Article  CAS  Google Scholar 

  • Hoffgaard IS, Ergon Å, Wanner LA, Tronsmo AM (2005) The effect of chitosan and bion on resistance to pink snow mould in perennial ryegrass and winter wheat. J Phytopathol 153:108–119

    Article  Google Scholar 

  • Howe GA (2005) Jasmonates as signals in the wound response. J Plant Regul 23:223–237

    Google Scholar 

  • Huckelhoven R, Kogel KH (2000) Association of hydrogen peroxide accumulation with expression of PR-1 during defense of barley against the powdery mildew fungus. Acta Phytopath Entomol Hungarica 35:231–238

    CAS  Google Scholar 

  • Huckelhoven R, Fodor J, Preis C, Kogel KH (1999) Hypersensitive cell death programme and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol 119:1251–1260

    Article  PubMed  CAS  Google Scholar 

  • Iriti M, Faoro F (2003) Benzothiadiazole (BTH) induces cell-death independent resistance in Phaseolus vulgaris against Uromyces appendiculatus. J Phytopathol 151:171–180

    Article  CAS  Google Scholar 

  • Iriti M, Faoro F (2006) Lipids biosynthesis in Spermatophyta. In: Teixeira DA, Silva JA (eds) Floriculture, ornamental and plant biotechnology, vol 1. Global Science Books, UK, pp 359–372

    Google Scholar 

  • Katz VA, Thulke OU, Conrath U (1998) A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiol 117:1333–1339

    Article  PubMed  CAS  Google Scholar 

  • Keogh RC, Deverall BJ, Mcleod S (1980) Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans Br Mycol Soc 74:329–333

    Article  Google Scholar 

  • Kiràly Z, El-Zahaby HM (2000) Effect of reactive oxygen species on rust and powdery mildew pathogens and on symptoms. Acta Phytopatol Entomol Hung 35:239–240

    Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Koga H, Bushnell WR, Zeyen RJ (1990) Specificity of cell type and timing of events associated with papilla formation and the hypersensitive reaction in leaves of Hordeum vulgare attacked by Erisiphe graminis f. sp. hordei. Can J Bot 68:2344–2352

    Google Scholar 

  • Kogel KH, Ortel B, Jarosch B, Atzorn R, Schiffer R, Wasternack C (1995) Resistance in barley against the powdery mildew fungus (Erysiphe graminis f. sp. hordei) is not associated with enhanced levels of endogenous jasmonates. Eur J Plant Pathol 101:319–332

    Article  CAS  Google Scholar 

  • Kramell R, Miersch O, Atzorn R, Parthier B, Wasternack C (2000) Octadecanoid-derived alteration of gene expression and the “oxylipin signature” in stressed barley leaves. Implications for different signaling pathways. Plant Physiol 123:177–187

    Article  PubMed  CAS  Google Scholar 

  • Kruger WM, Carver TLW, Zeyen RJ (2002) Phenolic inhibition of penetration resistance to Blumeria Graminis f. sp. hordei in barley near isogenic lines containing seven independent resistance genes or alleles. Physiol Mol Plant Pathol 61:41–51

    CAS  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signalling pathways in pathogen defense. Current Opin Plant Biol 31:631–645

    Google Scholar 

  • Kunz W, Schurter R, Maerzke T (1997) The chemistry of benzothiadiazole plant activators. Pest Sci 50:275–282

    Article  CAS  Google Scholar 

  • Lawton K, Friedrich L, Hunt M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J (1996) Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10:71–82

    Article  PubMed  CAS  Google Scholar 

  • Lumbroso E, Fischebeck G, Wahl I (1982) Infection of barley with conidia suspensions of Erysiphae graminis f. sp. hordei. Phytopath Z 104:222–233

    Google Scholar 

  • O’Brain TP, Feder N, Mc Cully ME (1964) Polycromatic staining of plant cell walls by toluidine blue. Protoplasma 59:367–373

    Google Scholar 

  • Reeve RM (1959) Histological and histochemical changes in developing and ripening peaches. I. The Catechol Tannins. Am J Bot 46:210–217

    Article  CAS  Google Scholar 

  • Scarponi L, Buonaurio R, Martinetti L (2001) Persistence translocation of a benzothiadiazole derivative in tomato plants in relation to systemic acquired resistance against Pseudomonas syringe pv tomato. Pest Manage Sci 57:262–268

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stadnik MJ, Buchenauer H (1999) Accumulation of autofluorogenic compounds at the penetration site of Blumeria graminis f. sp. tritici is associated with both benzothiadiazole-induced and quantitative resistance of wheat. J Phytopathol 147:615–622

    Article  CAS  Google Scholar 

  • Stadnik MJ, Buchenauer H (2000) Inhibition of phenylalanine ammonia-lyase suppresses the resistance induced by benzothiadiazole in wheat to Blumeria graminis f. sp. tritici. Physiol Mol Plant Pathol 57:25–34

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Thordal-Christensen H, Gregersen PL, Collinge DB (2000) The barley/Blumeria (syn. Erysiphe) graminis interaction: a case study. In: Slusarenko A, Fraser R, van Loon K (eds) Mechanisms of resistance to plant diseases. Kluwer Academic Publishers, Dordrecht, pp 77–100

    Google Scholar 

  • Vallélian-Bindschedler L, Metraux JP, Schweizer P (1998) Salicylic acid accumulation in barley is pathogen specific but not required for defense-gene activation. Mol Plant–Microbe Interact 11:702–705

    Article  Google Scholar 

  • 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. J Biol Chem 723:9013–9022

    Article  Google Scholar 

  • Vörös K, Feussner I, Kühn H, Lee J, Graner A, Löbler M, Parthier B, Wasternack C (1998) Characterization of a methyljasmonate-inducible lipoxygenase from barley (Hordeum vulgare cv. Salome) leaves. Eur J Biochem 251:36–44

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

We thank Prof. S. Lurie for critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Franco Faoro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Faoro, F., Maffi, D., Cantu, D. et al. Chemical-induced resistance against powdery mildew in barley: the effects of chitosan and benzothiadiazole. BioControl 53, 387–401 (2008). https://doi.org/10.1007/s10526-007-9091-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-007-9091-3

Keywords

Navigation