Abstract
Foliar application of Bacillus subtilis strain AUBS1 significantly reduced the sheath blight disease of rice (Oryza sativa L.) under greenhouse conditions. Treatment with B. subtilis led to an increase in the activities of phenylalanine ammonia-lyase (PAL) and peroxidase (PO) and an accumulation of pathogenesis-related (PR) proteins in rice leaves. Application of B. subtilis also induced an accumulation of a thaumatin-like protein (17 kDa) and two ß-1-3-glucanases (30 kDa and 33 kDa). Western blotting analysis for chitinase revealed the induction of two chitinases with apparent molecular masses of 30 kDa and 35 kDa in the induced plants. The coordinate upregulation of different defense mechanisms in induced plants suggests that these defense responses may be involved in the restriction of Rhizoctonia solani.
Zusammenfassung
Blattapplikation von Bacillus subtilis Stamm AUBSl reduzierte unter Gewächshausbedingungen die durch Rhizoctonia solani verursachte Blattscheidendürre an Reis (Oryza sativa L.). Behandlung mit B. subtilis führte zu einer Zunahme der Aktivitäten von Phenylalaninammonium-Lyase (PAL) und Peroxidase (PO) sowie zu einer Akkumulation von Pr-Proteinen in Reisblättern. Ferner wurde die Zunahme eines Thaumatin ähnlichen Proteins (17 kDa) und von zwei ß-1,3-Glucanasen (30 kDa und 33 kDa) induziert. Durch die western blotting-Analyse für Chitinasen konnte die Induktion von zwei Chitinasen mit den molekularen Massen von 30 kDa und 35 kDa nachgewiesen werden. Die koordinierte Regulierung von verschiedenen Abwehrmechanismen in induzierten Pflanzen deutet darauf hin, dass diese Abwehrreaktionen an der Restriktion von Rhizoctonia solani beteiligt sind.
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Literature
Bargabus, R. L., N. K. Zidack, J. E. Sherwood, B. J. Jacobsen: Characterization of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. — Physiol. Molec. Pl. Path. 61, 289–298, 2002.
Bochow, H., S. Dolej, I. Fischer, A. Melkamu: Plant health promoting effects by Bacillus subtilis and its mode of action. — In: Lyr, H, P. E. Russell, H. D. Sisler (eds.): Modern fungicides and antifungal compounds, pp. 549–554. Intercept Ltd. Andover, Hampshire, UK, 1996.
Buchenauer, H.: Biological control of soil-borne diseases by rhizobacteria. — Z. PflKrankh. PflSchutz. 105, 329–348, 1998.
Cho, S. J., S. K. Lee, B. J. Cha, Y. H. Kim, K. S. Shin: Detection and characterization of the Gloeosporium gloeosporioides growth inhibitory compound iturin A from Bacillus subtilis strain Ks03. — Fems Microbiol. Lett. 223, 47–51, 2003.
Collins, D. P., B. J. Jacobsen, B. Maxwell: Spatial and temporal population dynamics of a phyllosphere colonizing Bacillus subtilis biological control agent of sugar beet cercospora leaf spot. — Biol. Control 26, 224–232, 2003.
Datta, S. K., S. Muthukrishnan. Pathogenesis-related proteins in plants. — Crc Press, Boca Raton, USA, 1999.
Dickerson, D. P., S. F. Pascholati, A. E. Hagerman, L. G. Butler, R. L. Nicholson: Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. — Physiol. Pl. Path. 25, 111–123, 1984.
Emmert, E. A. B., J. Handelsman: Biocontrol of plant disease: a (Gram-) positive perspective. — Fems Microbiol. Lett. 171, 1–9, 1999.
Estevez-de-Jensen, C., J. A. Percich, P. H. Graham: Integrated management strategies of bean root rot with Bacillus subtilis and Rhizobium in Minnesota. — Field Crops Res. 74, 107–115, 2002.
Gupta, V. P., H. Bochow, S. Dolej, I. Fischer: Plant growth-promoting Bacillus subtilis strain as potential inducer of systemic resistance in tomato against Fusarium wilt. — J. Pl. Dis. Prot. 107, 145–154, 2000.
Hahlbrock, K., D. Scheel: Physiology and molecular biology of phenylpropanoid metabolism. — A. Rev. Pl. Physiol. Pl. Mol. Biol. 40, 347–369, 1989.
Hammerschmidt, R.: Induced disease resistance: How do induced plants stop pathogens? — Physiol. Molec. Pl. Path. 55, 77–84, 1999.
Hammerschmidt, R., E. M. Nuckles, J. Kuc: Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. — Physiol. Pl. Path. 20, 73–82, 1982.
Handelsman, J., S. Raffel, E. H. Mester, L. Wunderlich, C. R. Grau: Biological control of damping-off of alfalfa seedlings with Bacillus cereus Uw85. — Appl. Environ. Microbiol. 56, 713–718, 1990.
Havir, E. A., K. R. Hanson: L-phenylalanine ammonia-lyase. I. Purification and molecular size of the enzyme from potato tubers. — Biochemistry 7, 1896–1903, 1968.
Heil, M., R. M. Bostock: Induced systemic resistance (Isr) against pathogens in the context of induced plant defenses. — Annal. Bot. 89, 503–512, 2002.
Helbig, J.: Biological control of Botrytis cinerea Pers. ex Fr. in strawberry by Paenibacillus polymyxa (isolate 18191). — J. Phytopath. 149, 265–273, 2001.
Helbig, J., H. Bochow: Effectiveness of Bacillus subtilis (isolate 25021) in controlling Botrytis cinerea in strawberry. — J. Pl. Dis. Prot. 108, 545–559, 2001.
Hwang, S. F., K. F. Chang, R. J. Howard, B. A. Deneka, G. D. Turnbull: Decrease in incidence of Pythium damping-off of field pea by seed treatment with Bacillus spp. and metalaxyl. — J. Pl. Dis. Prot. 103, 31–41, 1996.
Hynes, R. K., G. Lazarovits: Effect of seed treatment with plant growth-promoting rhizobacteria on the protein profiles of intercellular fluids from bean and tomato leaves. — Can. J. Pl. Path. 11, 191, 1989.
Innocenti, G., R. Roberti, M. Montanari, E. Zakrisson: Efficacy of microorganisms antagonistic to Rhizoctonia cerealis and their cell wall-degrading enzymatic activities. — Mycol. Res. 107, 421–427, 2003.
Jayaraj, J., A. Anand, S. Muthukrishnan: Pathogenesis-Related proteins and their roles in resistance to fungal pathogens. — In: Punja, Z. K. (ed.): Fungal disease resistance in plants: Biochemistry, molecular biology and genetic engineering, pp. 177–230. Haworth Press, Ny, USA, 2003 (In Press).
Kannan, R., J. Jayaraj: Effect of various levels of inoculation of Bacillus subtilis on the incidence of damping-off of tomato and on plant growth parameters. — Annamalai Univ. Agric. Res. Annu. 21, 24–27, 1998.
Kim, D. S., R. J. Cook, D. M. Weller: Bacillus sp. L324-92 for biological control of three root diseases of wheat grown with reduced tillage. — Phytopathology 87, 551–558, 1997.
Laemmli, U. K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. — Nature 277, 680–684, 1970.
Lawrence, C. B., M. H. A. J. Joosten, S. Tuzun: Differential induction of pathogenesis-related proteins in tomato by Alternaria solani and the association of a basic chitinase isozyme with resistance. — Physiol. Molec. Pl. Path. 48, 361–377, 1996.
Leeman, M., J. A. van Pelt, M. J. Hendrickx, R. J. Scheffer, P. A. H. M. Bakker, B. Schippers: Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. — Phytopathology 85, 1301–1305, 1995.
M—Piga, P., R. R. Belanger, T. C. Paulitz, N. Benhamou: Increased resistance to Fusarium oxysporum f. sp. radicis lycopersici in tomato plants treated with endophytic bacterium Pseudomonas fluorescens strains 63–28. — Physiol. Molec. Pl. Path. 50, 301–320, 1997.
Manandhar, H. K., H. J. L. Jorgensen, S. B. Mathur, V. Smedegaard-Petersen: Suppression of rice blast by preinoculation with avirulent Pyricularia oryzae and the nonrice pathogen Bipolaris sorokiniana. — Phytopathology 88, 735–739, 1998.
Maplestone, P. A., R. Campbell: Colonization of roots of wheat seedlings by Bacilli proposed as biocontrol agents against take-all. — Soil Biol. Biochem. 21, 543–550, 1989.
Marten, P., K. Smalla, G. Berg: Genotypic and phenotypic differentiation of an antifungal biocontrol strain belonging to Bacillus subtilis. — J. Appl. Microbiol. 89, 463–471, 2000.
Massala, R., M. Legrand, B. Fritig: Effect of a-amino-oxy acetate, a competitive inhibitor of phenylalanine ammonia-lyase, on the hypersensitive resistance of tobacco to tobacco mosaic virus. — Physiol. Pl. Path. 16, 213–226, 1980.
Maurhofer, M., C. Hase, P. Meuwly, J. P. Metraux, G. Defago: Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain Chao: Influence of the gacA gene and of pyoverdine production. — Phytopathology 84, 139–146, 1994.
Meena, B., R. Radhajeyalakshmi, T. Marimuthu, P. Vidhyasekaran, S. Doraiswamy, R. Velazahan: Induction of pathogenesis-related proteins, phenolics and phenylalanine ammonia-lyase in groundnut by Pseudomonas fluorescens. — J. Pl. Dis. Prot. 107, 514–527, 2000.
Merriman, P. R., R. D. Price, J. F. Kollmorgen, T. Piggott, E. H. Ridge: Effect of seed inoculation with Bacillus subtilis and Streptomyces griseus on the growth of cereals and carrots. — Aust. J. Agric. Res. 25, 219–226, 1974.
Niranjan, R. S., S. A. Deepak, P. Basavaraju, H. S. Shetty, M. S. Reddy, J. W. Kloepper: Comparative performance of formulations of plant growth-promoting rhizobacteria in growth promotion and suppression of downy mildew in pearl millet. — Crop Prot. 22, 579–588, 2003.
Podile, A. R., V. D. V. Laxmi: Seed bacterization with Bacillus subtilis Af1 increases phenylalanine ammonia-lyase and reduces the incidence of Fusarial wilt in pigeonpea. — J. Phytopath. 146, 255–259, 1998.
Podile, A. R., G. S. Prasad, H. C. Dube: Partial characterization of the antagonistic principle of Bacillus subtilis Af1. — J. Biol. Control 1, 60–65, 1987.
Ramamoorthy, V., T. Raguchander, R. Samiyappan: Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. — Pl. Soil 239, 55–68, 2002.
Reimmann, C., R. Dudler: cDNA cloning and sequence analysis of a pathogenesis-related thaumatin-like protein from rice (Oryza sativa). — Pl. Physiol. 101, 1113–1114, 1993.
Sailaja, P. R., A. R. Podile, P. Reddanna: Biocontrol strain of Bacillus subtilis Af1 rapidly induces lipoxygenase in groundnut (Arachis hypogaea L.) compared to crown rot pathogen Aspergillus niger. Eur. J. Pl. Path. 104, 125–132, 1997.
SAS Institute: Sas System Version 7 for windows. — Sas Institute, Cary, NC, 1998.
Schlumbaum, A., F. Mauch, U. Vogeli, T. Boller: Plant chitinases are potent inhibitors of fungal growth. — Nature 324, 365–367, 1986.
Schmiedeknecht, G., H. Bochow, H. Junge: Use of Bacillus subtilis as biocontrol agent. II. Biological control of potato diseases. — J. Pl. Dis. Prot. 105, 376–386, 1998.
Schmiedeknecht, G., I. Issoufou, H. Junge, H. Bochow: Use of Bacillus subtilis as biocontrol agent. V. Biological control of diseases on maize and sunflowers. — J. Pl. Dis. Prot. 108, 500–512, 2001.
Sharma, N. R., P. S. Teng, F. M. Olivares: Comparison of assessment methods for rice sheath blight disease. — Philippine Phytopath. 26, 20–24, 1990.
Smith, P. K., R. I. Krohn, G. T. Hermanson, A. K. Maallia, F. H. Gartner, M. D. Provenzano, E. K. Fujimoto, N. M. Goeke, B. J. Olson, D. C. Klenk: Measurement of protein using bicinchoninic acid. — Anal. Biochem. 150, 76–85, 1985.
Someya, N., M. Nakajima, T. Hibi, I. Yamaguchi, K. Akutsu: Induced resistance to rice blast by antagonistic bacterium, Serratia marcescens strain B2. — J. Gen. Pl. Path. 68, 177–182, 2002.
Stadnik, M. J., H. Buchenauer: Inhibition of phenylalanine ammonia-lyase suppresses the resistance induced by benzothiadiazole in wheat to Blumeria graminis f. sp. tritici. — Physiol. Molec. Pl. Path. 57, 25–34, 2000.
Swegle, M., K. J. Kramer, S. Muthukrishnan: Properties of barley seed chitinases and release of embryo-associated isoforms during early stages of inhibition. — Pl. Physiol. 99, 1009–1014, 1992.
Van Loon, L. C., P. A. H. M. Bakker, C. M. J. Pieterse: Systemic resistance induced by rhizosphere bacteria. — A. Rev. Phytopath. 36, 453–483, 1998.
Velazhahan, R., K. C. Cole, C. S. Anuratha, S. Muthukrishnan: Induction of thaumatin-like proteins (TLPs) in Rhizoctonia solani-infected rice and characterization of two new cDna clones. — Physiologia Pl. 102, 21–28, 1998.
Velazhahan, R., S. K. Datta, S. Muthukrishnan: The Pr-5 family: Thaumatin-like proteins. — In: Datta, S. K., S. Muthukrishnan (eds.): Pathogenesis-related proteins in plants, pp. 107–129. Crc Press, Florida, USA, 1999.
Vidhyasekaran, P., N. Kamala, A. Ramanathan, K. Rajappan, V. Paranidharan, R. Velazhahan: Induction of systemic resistance by Pseudomonas fluor es cens Pf1 against Xanthomonas oryzae pv. oryzae in rice leaves. — Phytoparasitica 29, 155–166, 2001.
Zdor, R. E., A. J. Anderson: Influence of root colonizing bacteria on defense responses of bean. — Pl. Soil 140, 99–107, 1992.
Zhang, J.: Suppression of Fusarium colonization of cotton roots and Fusarium wilt by seed treatments with Gliocladium virens and Bacillus subtilis. — Biocontrol Sci. Technol. 6, 175–188, 1996.
Zheng, X. Y., J. B. Sinclair: The effects of traits of Bacillus megaterium on seed and root colonization and their correlation with the suppression of Rhizoctonia root rot of soybean. — Biocontrol 45, 223–243, 2000.
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Jayaraj, J., Yi, H., Liang, G.H. et al. Foliar application of Bacillus subtilis AUBS1 reduces sheath blight and triggers defense mechanisms in rice. J Plant Dis Prot 111, 115–125 (2004). https://doi.org/10.1007/BF03356138
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DOI: https://doi.org/10.1007/BF03356138
Key words
- Bacillus subtilis
- induced resistance
- Oryza sativa
- pathogenesis-related proteins
- peroxidase
- phenylalanine ammonia-lyase
- Rhizoctonia solani
- sheath blight