Abstract
Bacillussubtilis is well known for its biocontrol activity against several plant pathogens and for its role in promoting plant growth. HpaGXooc, from rice pathogenic bacterium Xanthomonasoryzae pv. oryzicola, is a member of the harpin group of proteins. It is known to elicit hypersensitive cell death in non-host plants, thereby inducing disease and insect resistance in the plants and enhancing plant growth. In our previous experiment, we constructed a genetically engineered strain—B. subtilis OKBHF—through the introduction of the gene encoding HpaGXooc into B. subtilis OKB105 in order to combine the effects of HpaGXooc and wild-type PGPR in improving the plant growth rate and for biological control. In this study, we evaluated the use of treating the tomato plant with B. subtilis OKBHF. The results of greenhouse experiments demonstrated that OKBHF treatment had a significant effect on increasing the height, fresh weight, and flower and fruit number and obviously lowered the disease severity of Cucumber mosaic virus (CMV) infection at 28 days postinoculation (dpi). Subsequent reverse transcription-polymerase chain reaction analysis revealed the molecular mechanisms of HpaGXooc and B. subtilis in the tomato plant, suggesting their synergistic roles in inducing enhanced expression of three expansin genes LeEXP2, LeEXP5, and LeEXP18, which regulate plant cell growth, and two defense-related genes Pti4 and Pti6, which activate the expression of a wide array of PR genes and one defense gene, PR-1a.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asaka O, Shoda M (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62:4081–4085
Choi D, Lee Y, Cho HT, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398
Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149
Dong HP, Peng J, Bao Z, Meng X, Bonasera JM, Chen G, Beer SV, Dong H (2004) Downstream divergence of the ethylene signaling pathway for harpin-stimulated Arabidopsis growth and insect defense. Plant Physiol 136:3628–3638
Dong HP, Yu H, Bao Z, Guo X, Peng J, Yao Z, Chen G, Qu S, Dong H (2005) The ABI2-dependent abscisic acid signalling controls HrpN-induced drought tolerance in Arabidopsis. Planta 221:313–327
Idris EE, Bochow H, Ross H, Borriss R (2004) Use of Bacillus subtilis as biocontrol agent. VI. Phytohormone like action of culture filtrates prepared from plant growth-promoting Bacillus amyloliquefaciens FZB24, FZB42, FZB45 and Bacillus subtilis FZB37. Zeitschrift fuer Pflanzenkrankheiten und Pflanzenschutz 111:583–597
Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borriss R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148:2097–2109
Kloepper JW, Ryu CM, Zhang S (2004a) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266
Kloepper JW, Reddy MS, Kenney DS, Vavrina C, Kokalis-Burelle N, Martinez-Ochoa N (2004b) Application for rhizobacteria in transplant production and yield enhancement. In: Nicola S, Nowak J, Vavrina CS (eds) XXVI International horticultural congress: issues and advances in transplant production and stand establishment research, Toronto, Canada, Acta Hort, vol 631, pp 219–229
Krause MS, De Ceuster TJ, Tiquia SM, Michel FC, Madden LV, Hoitink HA (2003) Isolation and characterization of rhizobacteria from composts that suppress the severity of bacterial leaf spot of radish. Phytopathology 93:1292–1300
Landy M, Warren GH, Rosenman SB, Colio LG (1948) Bacillomycin; an antibiotic from Bacillus subtilis active against pathogenic fungi. Proc Soc Exp Biol Med 67:539–541
Ma LL, Huo R, Gao XW, He D, Shao M, Wang Q (2008) Transgenic rape with hrf2 gene encoding harpinXooc resistant to Sclerotinia sclerotinorium. J Agric Sci China 7:455–461
Nandakumar R, Babu S, Viswanathan R, Raguchander T, Samiyappan R (2001) Induction of systemic resistance in rice against sheath blight disease by Pseudomonas fluorescens. J Soil Biol Biochem 33:603–612
Ongena M, Duby F, Jourdan E, Beaudry T, Jadin V, Dommes J, Thonart P (2005) Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl Microbiol Biotechnol 67:692–698
Peng JL, Dong HS, Dong HP, Delaney TP, Bonasera JM, Beer SV (2003) Harpin-elicited hypersensitive cell death and pathogen resistance require the NDR1 and EDS1 genes. Physiol Mol Plant Pathol 62:317–326
Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026
Saravanakumar D, Vijayakumar C, Kumar N, Samiyappan R (2007) PGPR-induced defense responses in the tea plant against blister blight disease. Crop Prot 26:556–565
Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18:555–561
Touré Y, Ongena M, Jacques P, Guiro A, Thonart P (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96:1151–1160
van Loon LC, Bakker PA, Pieterse CM (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483
Vollenbroich D, Pauli G, Ozel M, Vater J (1997) Antimycoplasma properties and application in cell culture of surfactin, a lipopeptide antibiotic from Bacillus subtilis. Appl Environ Microbiol 63:44–49
Wang S, Wu HJ, Qiao JQ, Ma LL, Liu J, Xia YF, Gao XW (2009) Molecular mechanism of plant growth promotion and induced systemic resistance to tobacco mosaic virus by Bacillus spp. J Microbiol Biotechnol 19:1250–1258
Wu K, Tian L, Hollingworth J, Brown DC, Miki B (2002) Functional analysis of tomato Pti4 in Arabidopsis. Plant Physiol 128:30–37
Wu HJ, Wang S, Qiao JQ, Liu J, Zhan J, Gao XW (2009) Expression of HpaGXooc protein in Bacillus subtilis and its biological functions. J Microbiol Biotechnol 19:194–203
Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395
Acknowledgments
This work was supported by grants from National Natural Science Fund of China (30570041), the National 863 Program of China (2006AA10Z172; 2006AA10A203), the Special Nonprofit Scientific Research Program, P. R. China (3-32), Program of International Science and Technology Cooperation (2009DFA32740), the Specialized Research Fund for the Doctoral Program of Higher Education, P. R. China (20060307012), and Youth Science and Technology Innovation Fund of Nanjing Agricultural University (KJ09007).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Reijo Karjalainen.
Authors Shuai Wang and Huijun Wu contributed equally to this work and are regarded as joint first authors.
Rights and permissions
About this article
Cite this article
Wang, S., Wu, H., Zhan, J. et al. The role of synergistic action and molecular mechanism in the effect of genetically engineered strain Bacillus subtilis OKBHF in enhancing tomato growth and Cucumber mosaic virus resistance. BioControl 56, 113–121 (2011). https://doi.org/10.1007/s10526-010-9306-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-010-9306-x