ANTAGONISTIC ACTIVITY OF PLANT-ASSOCIATED MICROORGANISMS AGAINST Phytophthora infestans
Hanna Rekosz-Burlaga
Warsaw University of Life SciencesEdyta Tokarczyk
Warsaw University of Life SciencesJarosław Szczepaniak
Warsaw University of Life SciencesAgata Goryluk-Salmonowicz
Warsaw University of Life SciencesAbstract
Phytophthora infestans is a pathogen threatening potato and tomato tillages. Environmentally safe biological methods are searched for the prevention against this
pathogen. Many biocontrolling agents occur in plants or on their surfaces. Our studies were aimed at searching for effective antagonists against P. infestans among the isolates of endophyte and epiphyte bacteria. 37 endophyte and 26 epiphyte bacterial strains isolated from Equisetum arvense, Elymus repens and Chenopodium album L. were studied. The bacterial strains were screened for their antagonistic activity against Phytophthora infestans. The inhibitory effect of the bacteria was estimated based on the calculation of the per cent of relative growth. All tested isolates showed antagonistic properties against P. infestans. The strongest activity was observed for the B. subtilis strain. Plant species and the tested parts of the plants had an important influence on the antagonistic activity of bacterial strains isolated from these plants. The endophyte growth rate inhibition of P. infestans was higher than for the epiphyte strains and was over 40% for most isolates. Bacterial biocontrolling agents should be searched among endophytes of the studied plants and not among bacteria colonizing their phyllosphere.
Keywords:
endophytes, epiphytes, bacterial biocontrolling agents, blight of potato and tomatoReferences
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Daayf, F., Adam, L., Fernando, W.G.D. (2003). Comparative screening of bacteria for biological control of potato late blight (strain US-8), using in vitro, detached-leaves, and whole-plant testing systems. Can. J. Plant Pathol., 25, 276–284.
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Rekosz-Burlaga, H., Borys, M., Goryluk-Salmonowicz, A. (2014). Cultivable microorganisms inhabiting the aerial parts of Hypericum perforatum. Acta Sci. Pol. Hortorum Cultus, 13(5), 117–129.
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Sedláková, V., Dejmalová, J., Hausvater, E., Sedlák, P., Doležal, P., Mazáková, J. (2011). Effect of Phytophthora infestans on potato yield in dependence on variety characteristics and fungicide control. Plant Soil Environ., 57(10), 486–491.
Son, S.W., Kim, H.Y., Choi, G.J., Lim, H.K., Jang, K.S., Lee, S.O., Lee, S., Sung, N.D. (2008). Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against Phytophthora infestans. J. Appl. Microbiol., 104, 692–698.
Stephan, D., Schmitt, A., Martins Carvalho, S., Seddon, B., Koch, E. (2005). Evaluation of biocontrol preparations and plant extracts for the control of Phytophthora infestans on potato leaves. Eur. J. Plant Pathol., 112, 235–246.
Sunaina, V., Ajay, S. (2007). Evaluation of biocontrol agent Bacillus subtilis b5 for control of Phytophthora infestans on potato leaves. Potato J., 34(1–2), 79–80.
Tran, H., Ficke, A., Asiimwe, T., Höfte, M., Raaijmakers, J.M. (2007). Role of the cyclic lipopeptide massetolide a in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytolog., 175(4), 731–742.
Yang, Ch., Crowley, D.E., Borneman, J., Keen, N.T. (2000). Microbial phyllosphere populations are more complex than previously realized. PNAS, 98(7), 3889–3894.
Walker, R., Ferguson, C.M.J., Booth, N.A., Allan, J. (2002). The symbiosis of Bacillus subtilis L-forms with Chinese cabbage seedlings inhibits conidial germination of Botrytis cinerea. Lett. Appl. Microbiol. 34(1), 42–45.
Whipps, J.M., Hand, P., Pink, D., Bending, G.D. (2008). Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol., 105(6), 1744–1755.
Bacon, C.W., Yates, I.E., Hinton, D.M., Meredith, F. (2001). Biological control of Fusarium moniliforme in Maize. Environ Health Persp., 109(2), 325–332.
Beakes, G.W., Glockling, S.L., Sekimoto, S., 2012. The evolutionary phylogeny of the oomycete “fungi”. Protoplasma, 249(1), 3–19. doi: 10.1007/s00709-011-0269-2
Broggini, G.A.L., Duffy, B., Holliger, E., Schärer, H., Gessler, C., Patocchi, A. (2005). Detection of the fire blight biocontrol agent Bacillus subtilis BD170 (Biopro) in a Swiss apple orchard. Eur. J. Plant Pathol., 111(2), 93–100.
Cawoy, H., Bettiol, W., Fickers, P., Ongena, M. (2011). Bacillus – based biological control of plant diseases. In: Pesticides in the modern world – pesticides use and management, Stoytcheva, M. (ed.). Pub. InTech, 273–302.
Chandrakala, A., Chandrashekar, S.C., Jyothi, G., Ravikumar, B.M. (2012). Effect of cell-free culture filtrates of bio-control agents on the spore germination and infection by Phytophthora infestans causing late blight of potato. Glob. J. Biol. Agricult. Health Sci., 1(2), 40–45.
Cooke, D.E.L., Lees, A.K. (2004). Markers, old and new, for examining Phytophthora infestans diversity. Plant Pathol., 53, 692–704.
Daayf, F., Adam, L., Fernando, W.G.D. (2003). Comparative screening of bacteria for biological control of potato late blight (strain US-8), using in vitro, detached-leaves, and whole-plant testing systems. Can. J. Plant Pathol., 25, 276–284.
Esh, A.M., Atia, M.M.M., Tohamy, M.R.A., Taghian, S. (2011). Systemic resistance in sugar beet elucidated by non-pathogenic, phyllosphere-colonizing Bacillus pumilus and B. subtilus against the pathogen Cercospora beticola Sacc. J. Plant Protect. Pathol., 2(1), 67–83.
Gisi, U., Cohen, Y. (1996). Resistance to phenylamide fungicides: a case study with Phytophthora infestans involving mating type and race structure. Ann. Rev. Phytopath., 34, 549–572.
Griffith, J.M., Davis, A.J., Grant, B.R. (1992). Target sites of fungicides to control Oomtcetes. In: Target sites of fungicide action, Koller, W. (ed). London, CRC Press, 69–100.
Hallmann, J., Quadt-Hallmann, A., Mahaffee, W.F., Kloepper, J.W. (1997). Bacterial endophytes in agricultural crops. Can. J. Microbiol., 43(10), 895–914.
Hardham, A.R. (2005). Pathogen profile Phytophthora cinnamomi. Mol. Plant Pathol., 6(6), 589–604.
Jiyeon, L., Kwon, G.-H., Park, J.-Y., Park, C.-S., Kwon, D.Y., Lim, J., Kim, J.S., Kim, J.H. (2011). A RAPD-PCR Method for the rapid detection of Bacillus cereus. J. Microbiol. Biotechnol., 21(3), 274–276. doi: 10.4014/jmb.1008.08031
Judelson, H.S., Blanco, F.A. (2005). The spores of Phytophthora: weapons of the plant destroyer. Nat. Rev. Microbiol. 3, 4 7–58.
Jung, T., Burgess, T.I. (2009). Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia, 22, 95–110.
Kwon, G.H., Lee, H.A., Park, J.Y., Kim, J.S., Lim, J. (2009). Development of a RAPD-PCR method for identification of Bacillus species isolated from Cheonggukjang. Int. J. Food Microbiol., 129, 282–287.
Khabbaz, S.E., Zhang, L., Cáceres, L.A., Sumarah, M., Wang, A., Abbasi, P.A. (2015). Characterisation of antagonistic Bacillus and Pseudomonas strains for biocontrol potential and suppression of damping-off and root rot diseases. Ann. Appl. Biol., 1–16. doi: 10.1111/aab.12196
Lagace, L., Pitre, M., Jacques, M., Roy, D. (2004). Identification of the bacterial community of maple sap by using amplified ribosomal DNA (rDNA) restriction analysis and rDNA sequencing. Appl. Environ. Microbiol., 70(4), 2052–2060. doi: 10.1128/AEM.70.4.2052-2060
Logan, N.A., De Vos, P. (2009). Genus I. Bacillus Cohn 1872, 174AL. In: Bergey’s manual of systematic bacteriology, De Vos, P., Garrity, G.M., Jones, D., Krieg, N.R., Ludwig, W., Rainey, F.A., Schleifer, K.H., Whitman, W.B. (eds). 2nd Edition, Springer, New York, 3, 21–128.
Maksimov, I.V., Abizgildina, P.P., Sorokan’, A.V., Burkhanova, G.F. (2014). Regulation of peroxidase activity under the influence of signaling molecules and Bacillus subtilis 26D in potato plants infected with Phytophthora infestans. Appl. Biochem. Microbiol., 50(2), 197–202.
Moushib, L., Wtzell, J., Lenman, M., Liljeroth, E., Andreasson, E. (2013). Sugar beet extract induces defense against Phytophthora infestans in potato plants. Eur. J. Plant Pathol. 136(2), 261–271. doi: 10.1007/s10658-012-0160-9
Nelson, S.C. (2008). Late blight of tomato (Phytophthora infestans). Plant Disease, PD-45, 1–10.
Nongkhlaw, F.M.W., Joshi, S. R. (2014). Epiphytic and endophytic bacteria that promote growth of ethnomedicinal plants in the subtropical forests of Meghalaya, India. Home, 62(4). http://revistas.ucr.ac.cr/index.php/rbt/article/view/12138/15463
Patel, R.R., Thakkar, V.R., Subramanian, B.R. (2015). A Pseudomonas guariconensis strain capable of promoting growth and controlling collar rot disease in Arachis hypogaea L. Plant Soil, 390 (1), 369–381. doi 10.1007/s11104-015-2436-2
Pini, F., Galardini, M., Bazzicalupo, M., Mengoni, A. (2011). Plant-bacteria association and symbiosis: Are there common genomic traits in Alphaproteobacteria? Genes, 2, 1017–1032. doi:10.3390/genes2041017
Puopolo, G., Cimmino, A., Palmieri, M.C., Giovannini, O., Evidente, A., Pertot, I. (2014). Lysobacter capsici AZ78 produces cyclo(L-Pro-L-Tyr), a 2,5-diketopiperazine with toxic activity against sporangia of Phytophthora infestans and Plasmopara viticola. J. Appl. Microbiol., 117, 1168–1180.
Raaijmakers, J.M., Vlami, M., de Souza, J.T. (2002). Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek, 81, 537–547.
Rekosz-Burlaga, H., Borys, M., Goryluk-Salmonowicz, A. (2014). Cultivable microorganisms inhabiting the aerial parts of Hypericum perforatum. Acta Sci. Pol. Hortorum Cultus, 13(5), 117–129.
Schlenzig, A., Habermayer, J., Zinkernagel, V. (1999). Serological detection of latent infection with Phytophthora infestans in potato stems. Zeitschrift für Pflanzenkrankheiten und Pfl, 105(1), 22–33.
Sedláková, V., Dejmalová, J., Hausvater, E., Sedlák, P., Doležal, P., Mazáková, J. (2011). Effect of Phytophthora infestans on potato yield in dependence on variety characteristics and fungicide control. Plant Soil Environ., 57(10), 486–491.
Son, S.W., Kim, H.Y., Choi, G.J., Lim, H.K., Jang, K.S., Lee, S.O., Lee, S., Sung, N.D. (2008). Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against Phytophthora infestans. J. Appl. Microbiol., 104, 692–698.
Stephan, D., Schmitt, A., Martins Carvalho, S., Seddon, B., Koch, E. (2005). Evaluation of biocontrol preparations and plant extracts for the control of Phytophthora infestans on potato leaves. Eur. J. Plant Pathol., 112, 235–246.
Sunaina, V., Ajay, S. (2007). Evaluation of biocontrol agent Bacillus subtilis b5 for control of Phytophthora infestans on potato leaves. Potato J., 34(1–2), 79–80.
Tran, H., Ficke, A., Asiimwe, T., Höfte, M., Raaijmakers, J.M. (2007). Role of the cyclic lipopeptide massetolide a in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytolog., 175(4), 731–742.
Yang, Ch., Crowley, D.E., Borneman, J., Keen, N.T. (2000). Microbial phyllosphere populations are more complex than previously realized. PNAS, 98(7), 3889–3894.
Walker, R., Ferguson, C.M.J., Booth, N.A., Allan, J. (2002). The symbiosis of Bacillus subtilis L-forms with Chinese cabbage seedlings inhibits conidial germination of Botrytis cinerea. Lett. Appl. Microbiol. 34(1), 42–45.
Whipps, J.M., Hand, P., Pink, D., Bending, G.D. (2008). Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol., 105(6), 1744–1755.
Hanna Rekosz-Burlaga
Warsaw University of Life Sciences
Warsaw University of Life Sciences
Edyta Tokarczyk
Warsaw University of Life Sciences
Warsaw University of Life Sciences
Jarosław Szczepaniak
Warsaw University of Life Sciences
Warsaw University of Life Sciences
Agata Goryluk-Salmonowicz
Warsaw University of Life Sciences
Warsaw University of Life Sciences
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