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Suppressive efficacy of volatile compounds produced by Bacillus mycoides on damping-off pathogens of cabbage seedlings

Published online by Cambridge University Press:  24 September 2018

J.-S. Huang ,
Y.-H. Peng ,
K.-R. Chung  and
J.-W. Huang
J.-S. Huang
Affiliation:
Department of Plant Pathology, National Chung-Hsing University, Taichung 40227, Taiwan
Y.-H. Peng
Affiliation:
Department of Plant Pathology, National Chung-Hsing University, Taichung 40227, Taiwan
K.-R. Chung*
Affiliation:
Department of Plant Pathology, National Chung-Hsing University, Taichung 40227, Taiwan
J.-W. Huang
Affiliation:
Department of Plant Pathology, National Chung-Hsing University, Taichung 40227, Taiwan Innovation and Development Center of Sustainable Agriculture (IDCSA), Taichung 40227, Taiwan
*
Authors for correspondence: K.-R. Chung, E-mail: krchung@nchu.edu.tw and J.-W. Huang, E-mail: jwhuang@dragon.nchu.edu.tw
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Abstract

Rhizoctonia solani Kühn and Pythium aphanidermatum Edson cause cabbage seedling damping-off, resulting in severe yield losses. The current study demonstrates the production of toxic volatile organic compounds (VOCs) by two strains of Bacillus mycoides and the evaluation of a potential use of B. mycoides as a biocontrol agent to control cabbage damping-off. Two VOCs, dimethyl disulphide and ammonia, were found to reduce radial growth, cause hyphal deformation and result in organelle degeneration in both R. solani and P. aphanidermatum. Pathogen hyphae, after being exposed to VOCs, showed poor rigidity, shrinkage, curling and swelling. The amount of VOCs produced by B. mycoides and the antagonistic activity against plant pathogens varied, depending on the type of medium used to culture bacteria. Application of B. mycoides cell suspensions to cultivation medium promotes growth of five different plant species tested. Experiments conducted in greenhouses revealed that B. mycoides did not reduce damping-off incidence caused by R. solani. However, B. mycoides reduced damping-off incidence induced by P. aphanidermatum by as much as 45% on cabbage seedlings. The results provide valuable information on the feasibility of utilizing B. mycoides as a biocontrol agent in controlling cabbage damping-off.

Keywords

Ammoniadimethyl disulphidegas-producing bacteriumhyphal deformationrhizosphere
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 156 , Issue 6 , August 2018 , pp. 795 - 809
Copyright
Copyright © Cambridge University Press 2018 

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References

Adams, DJ (2004) Fungal cell wall chitinases and glucanases. Microbiology (Reading, England) 150, 2029–2035.Google Scholar
Anakwenze, VN, Ezemba, CC and Ekwealor, IA (2014) Improved cultural conditions for methionine accumulation in submerged cultivation of Bacillus cereus S8. British Microbiology Research Journal 4, 885–895.Google Scholar
Arrebola, E, Sivakumar, D and Korsten, L (2010) Effect of VOCs produced by Bacillus strains on postharvest decay in citrus. Biological Control 53, 122–128.Google Scholar
Atlas, RM (1993) Handbook of Microbiological Media. Boca Raton, FL, USA: CRC Press.Google Scholar
Audrain, B, Farag, MA, Ryu, CM and Ghigo, JM (2015) Role of bacterial VOCs in bacterial biology. FEMS Microbiology Review 39, 222–233.Google Scholar
Auger, J, Arnault, I, Diwo-Allain, S, Ravier, N, Molia, F and Pettiti, M (2004) Insecticidal and fungicidal potential of Allium substances as biofumigants. Agroindustria 3, 5–8.Google Scholar
Bargabus, RL, Zidack, NK, Sherwood, JE and Jacobsen, BJ (2004) Screening for the identification of potential biological control agents that induce systemic acquired resistance in sugar beet. Biological Control 30, 342–350.Google Scholar
Blaschek, W, Käsbauer, J, Kraus, J and Franz, G (1992) Pythium aphanidermatum: culture, cell-wall composition, and isolation and structure of antitumour storage and solubilised cell-wall (1-3)(1-6)-beta-D-glucans. Carbohydrate Research 231, 293–307.Google Scholar
Blom, D, Fabbri, C, Eberl, L and Weisskopf, L (2011) Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Applied and Environmental Microbiology 77, 1000–1008.Google Scholar
Buyer, JS (1995) A soil and rhizosphere microorganism isolation and enumeration medium that inhibits Bacillus mycoides. Applied and Environmental Microbiology 61, 1839–1842.Google Scholar
Chaurasia, B, Pandey, A, Palni, LM, Trivedi, P, Kumar, B and Colvin, N (2005) Diffusible and VOCs produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiological Research 160, 75–81.Google Scholar
Chen, JT, Lin, MJ and Huang, JW (2015) Efficacy of spent blewit mushroom compost and Bacillus aryabhattai combination on control of Pythium damping-off in cucumber. Journal of Agricultural Science, Cambridge 153, 1257–1266.Google Scholar
Cherif, A, Borin, S, Rizzi, A, Ouzari, H, Boudabous, A and Daffonchio, D (2002) Characterization of a repetitive element polymorphism-polymerase chain reaction chromosomal marker that discriminates Bacillus anthracis from related species. Journal of Applied Microbiology 93, 456–462.Google Scholar
Claeson, AS, Sandstrom, M and Sunesson, AL (2007) Volatile organic compounds (VOCs) emitted from materials collected from buildings affected by microorganisms. Journal of Environmental Monitoring 9, 240–245.Google Scholar
Claus, D and Berkeley, RCW (1986) Genus Bacillus chon 1872. In Sneath, PHA, Mair, NS, Sharpe, ME and Holt, JG (eds), Bergey's Manual of Systematic Bacteriology, vol. 2. Baltimore, USA: Williams and Wilkins, pp. 1105–1139.Google Scholar
Czaban, J, Ksiezniak, A, Wroblewska, B and Paszkowski, WL (2004 a) An attempt to protect winter wheat against Gaeumannomyces graminis var. tritici by the use of rhizobacteria Pseudomonas fluorescens and Bacillus mycoides. Polish Journal of Microbiology 53, 101–110.Google Scholar
Czaban, J, Ksiezniak, A and Paszkowski, W (2004 b) An attempt to protect winter wheat against Fusarium culmorum by the use of rhizobacteria Pseudomonas fluorescens and Bacillus mycoides. Polish Journal of Microbiology 53, 175–182.Google Scholar
Di Francesco, A, Ugolini, L, Lazzeri, L and Mari, M (2015) Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biological Control 81, 8–14.Google Scholar
Di Franco, C, Beccari, E, Santini, T, Pisaneschi, G and Tecce, G (2002) Colony shape as a genetic trait in the pattern-forming Bacillus mycoides. BMC Microbiology 2, 33.Google Scholar
Ding, PF and Huang, JW (2017) Identification and evaluation of Bacillus mycoides as a biocontrol agent for controlling tomato Fusarium wilt. Plant Medicine 59, 19–26, in Chinese.Google Scholar
Driks, A (2004) The Bacillus spore coat. Phytopathology 94, 1249–1251.Google Scholar
Edwards, RA, Dainty, RH and Hibbard, CM (1987) VOCs produced by meat pseudomonads and related reference strains during growth on beef stored in air at chill temperatures. Journal of Applied Bacteriology 62, 403–412.Google Scholar
Endoh, T, Kasuga, K, Horinouchi, M, Yoshida, H, Habe, H, Nojiri, H and Omori, T (2003) Characterization and identification of genes essential for dimethyl sulfide utilization in Pseudomonas putida strain DS1. Applied Microbiology and Biotechnology 62, 83–91.Google Scholar
Farag, MA, Ryu, CM, Sumner, LW and Pare, PW (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67, 2262–2268.Google Scholar
Fernando, WGD, Ramarathnam, R, Krishnamoorthy, AS and Savchuk, SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biology and Biochemistry 37, 955–964.Google Scholar
Fiddaman, PJ and Rossall, S (1993) The production of antifungal volatiles by Bacillus subtilis. Journal of Applied Bacteriology 74, 119–126.Google Scholar
Gardener, BBM and Driks, D (2004) Overview of the nature and application of biocontrol microbes: Bacillus spp. Phytopathology 94, 1244.Google Scholar
Howell, CR, Beier, RC and Stipanovic, RD (1988) Production of ammonia by Enterobacter cloacae and its possible role in the biological control of Pythium preemergence damping-off by the bacterium. Phytopathology 78, 1075–1078.Google Scholar
Hsieh, TY, Lin, TC, Lin, CL, Chung, KR and Huang, JW (2016) Reduction of Rhizoctonia damping-off in Chinese cabbage seedlings by fungal protein activators. Plant Medicine 58, 1–8.Google Scholar
Huang, CJ, Tsay, JF, Chang, SY, Yang, HP, Wu, WS and Chen, CY (2012) Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Management Science 68, 1306–1310.Google Scholar
Kai, M, Effmert, U, Berg, G and Piechulla, B (2007) Volatiles of bacteria; antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Archives of Microbiology 187, 351–360.Google Scholar
Kanchiswamy, CN, Malnoy, M and Maffei, ME (2015) Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends in Plant Science 20, 206–211.Google Scholar
Keinath, AP, Cubeta, MA and Langston, DB Jr (2006) Cabbage diseases, ecology and control. In Pimentel, D (ed.) Encyclopedia of Pest Management. New York, NY, USA: Taylor and Francis, pp. 1–4.Google Scholar
King, EO, Ward, MK and Raney, DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. Journal of Laboratory and Clinical Medicine 44, 301–307.Google Scholar
Li, Q, Ning, P, Zheng, L, Huang, J, Li, G and Hsiang, T (2012) Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biological Control 61, 113–120.Google Scholar
Meldau, DG, Meldau, S, Hoang, LH, Underberg, S, Wünsche, H and Baldwin, IT (2013) Dimethyl disulfide produced by the naturally associated bacterium bacillus sp. B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25, 2731–2747.Google Scholar
Pal, KK and Gardener, BM (2006) Biological control of plant pathogens. Plant Heath Instructor, doi: 10.1094/PHI-A-2006-1117-02.Google Scholar
Peng, YH, Chou, YJ, Liu, YC, Jen, JF, Chung, KR and Huang, JW (2017) Inhibition of cucumber Pythium damping-off pathogen with zoosporicidal biosurfactants produced by Bacillus mycoides. Journal of Plant Diseases and Protection 124, 481–491.Google Scholar
Petersen, DJ, Shishido, M, Holl, FB and Chanway, CD (1995) Use of species and strain-specific PCR primers for identification of conifer root associated Bacillus spp. FEMS Microbiology Letter 133, 71–76.Google Scholar
Rivas, R, Velázquez, E, Zurdo-Piñeiro, JL, Mateos, PF and Martínez Molina, E (2004) Identification of microorganisms by PCR amplification and sequencing of a universal amplified ribosomal region present in both prokaryotes and eukaryotes. Journal of Microbiological Methods 56, 413–426.Google Scholar
Ryu, CM, Farag, MA, Hu, CH, Reddy, MS, Klopper, JW and Paré, PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiology 134, 1017–1026.Google Scholar
Schulz, S and Dickschat, JS (2007) Bacterial volatiles: the smell of small organisms. Natural Product Reports 24, 814–842.Google Scholar
Shafi, J, Tian, H and Ji, M (2017) Bacillus species as versatile weapons for plant pathogens: a review. Biotechnology and Biotechnological Equipment 31, 446–459.Google Scholar
Siddiqui, ZA (2006) PGPR: Biocontrol and Biofertilization. Dordrecht, The Netherlands: Springer Publication.Google Scholar
Stephens, CT, Herr, LJ, Schmitthenner, AF and Powell, CC (1982) Characterization of Rhizoctonia isolates associated with damping-off bedding plants. Plant Disease 66, 700–703.Google Scholar
Stinson, M, Ezra, D, Hess, WM, Sears, J and Strobel, G (2003) An endophytic Gliocladium sp. of Eucryphia cordifolia producing selective volatile antimicrobial compounds. Plant Science 165, 913–922.Google Scholar
Vaughn, SF and Spencer, GF (1994) Antifungal activity of natural compounds against thiabendazole-resistant Fusarium sambucinum strains. Journal of Agricultural and Food Chemistry 42, 200–203.Google Scholar
Wan, M, Li, G, Zhang, J, Jiang, D and Huang, HC (2008) Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biological Control 46, 552–559.Google Scholar
Weise, T, Kai, M and Piechulla, B (2013) Bacterial ammonia causes significant plant growth inhibition. PLoS ONE 8, e63538.Google Scholar
Whipps, JM (2001) Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany 52(suppl. 1), 487–511.Google Scholar
Yamada, S, Ohashi, E, Agata, N and Venkateswaran, K (1999) Cloning and nucleotide sequence analysis of gyrB of Bacillus cereus, B. thuringiensis, B. mycoides, and B. anthracis and their application to the detection of B. cereus in rice. Applied and Environmental Microbiology 65, 1483–1490.Google Scholar