[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.4014/jmb.0901.008

Molecular Mechanism of Plant Growth Promotion and Induced Systemic Resistance to Tobacco Mosaic Virus by Bacillus spp.

Wang, Shuai (Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture)
Wu, Huijun (Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture)
Qiao, Junqing (Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture)
Ma, Lingli (Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture)
Liu, Jun (Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture)
Xia, Yanfei (Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture)
Gao, Xuewen (Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture)

Publication Information

Journal of Microbiology and Biotechnology / v.19, no.10, 2009 , pp. 1250-1258 More about this Journal

Abstract

Bacillus spp., as a type of plant growth-promoting rhizobacteria (PGPR), were studied with regards promoting plant growth and inducing plant systemic resistance. The results of greenhouse experiments with tobacco plants demonstrated that treatment with the Bacillus spp. significantly enhanced the plant height and fresh weight, while clearly lowering the disease severity rating of the tobacco mosaic virus (TMV) at 28 days post-inoculation (dpi). The TMV accumulation in the young non-inoculated leaves was remarkably lower for all the plants treated with the Bacillus spp. An RT-PCR analysis of the signaling regulatory genes Coil and NPR1, and defense genes PR-1a and PR-1b, in the tobacco treated with the Bacillus spp. revealed an association with enhancing the systemic resistance of tobacco to TMV. A further analysis of two expansin genes that regulate plant cell growth, NtEXP2 and NtEXP6, also verified a concomitant growth promotion in the roots and leaves of the tobacco responding to the Bacillus spp.

Keywords

Bacillus spp; PGPR; induced systemic resistance; tobacco mosaic virus; growth promotion;

Citations & Related Records

Times Cited By Web Of Science : 4 (Related Records In Web of Science)

Reference

1	Choi, D., Y. Lee, H. T. Cho, and H. Kende. 2003. Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15: 1386-1398 DOI ScienceOn
2	Clarke, J. D., N. Aarts, B. J. Feys, X. Dong, and J. E. Parker. 2000. Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12: 2175-2190 DOI ScienceOn
3	Dangl, J. L. and J. D. Jones. 2001. Plant pathogens and integrated defense responses to infection. Nature 411: 826-833 DOI ScienceOn
4	Dobbelaere, S., J. Vanderleyden, and Y. Okon. 2003. Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit. Rev. Plant Sci. 22: 107-149 DOI ScienceOn
5	Dong, X. 1998. SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1: 316-323 DOI PUBMED ScienceOn
6	Kloepper, J. W., C. M. Ryu, and S. Zhang. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94: 1259-1266 DOI ScienceOn
7	Kloepper, J. W., F. M. Scher, M. Laliberte, and B. Tipping. 1986. Emergence-promoting bacteria: Description and implications for agriculture, pp. 155-164. In T. R. Swinburne (ed.). Iron, Siderphores and Plant Diseases. Plenum, New York
8	Krause, M. S., T. J. J. De Ceuster, S. M. Tiquia, F. C. Michel, Jr. L. V. Madden, and H. A. J. Hoitink. 2003. Isolation and characterization of rhizobacteria from composts that suppress the severity of bacterial leaf spot of radish. Phytopathology 93:1292-1300 DOI ScienceOn
9	Landy, M., G. H. Warren, S. B. Roseman, and L. G. Colio. 1948. Bacillomycin, an antibiotic from Bacillus subtilis active against pathogenic fungi. Proc. Soc. Exp. Biol. Med. 67: 539-541
10	Maurhofer, M., C. Hase, P. Meuwly, J. P. Metraux, and G. Defago. 1994. Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: Influence of the gacA gene and of pyoverdine production. Phytopathology 84: 139-146 DOI ScienceOn
11	Mou, Z., W. Fan, and X. Dong. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 815-826 DOI PUBMED ScienceOn
12	Wang, Y., Y. Ohara, H. Nakayashiki, Y. Tosa, and S. Mayama. 2005. Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol. Plant Microbe Interact. 18: 385-396 DOI ScienceOn
13	Zhang, S., M. S. Reddy, and J. W. Kloepper. 2004. Tobacco growth enhancement and blue mold disease protection by rhizobacteria: Relationship between plant growth promotion and systemic disease protection by PGPR strain 90-166. Plant Soil 262: 277-288 DOI ScienceOn
14	Krebs, B., B. Hoding, S. M. Kubart, A. Workie, H. Junge, G. Schmiedeknecht, R. Grosch, H. Bochow, and M. Hevesi. 1998. Use of Bacillus subtilis as biocontrol agent. 1. Activities and characterization of Bacillus subtilis strains. J. Plant Dis. Prot. 105: 181-197
15	Cao, H., J. Glazebrook, J. D. Clarke, S. Volko, and X. Dong. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-63 DOI ScienceOn
16	Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A
17	Schmiedeknecht, G., H. Bochow, and H. Junge. 1998. Use of Bacillus subtilis as biocontrol agent. II. Biological control of potato disease. J. Plant Dis. Prot. 105: 376-386
18	Idris, E. E. S., H. Bochow, H. Ross, and R. Borriss. 2004. Use of Bacillus subtilis as biocontrol agent. Phytohormone-like action of culture filtrates prepared from plant growth-promoting Bacillus amyloliquefaciens FZB24, FZB42, FZB45 and Bacillus subtilis FZB37. J. Plant Dis. Prot. 111: 583-597
19	Zehnder, G. W., C. Yao, J. F. Murphy, E. R. Sikora, and J. W. Kloepper. 2000. Induction of resistance in tomato against cucumber mosaic cucumovirus by plant growth-promoting rhizobacteria. Biocontrol 45: 127-137 DOI ScienceOn
20	Pieterse, C. M. J., S. C. M. van Wees, J. A. van Pelt, M. L. R. Knoester, H. Gerrits, P. J. Weisbeek, and L. C. van Loon. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10: 1571–1580 DOI PUBMED ScienceOn
21	Saravanakumara, D., V. Charles, N. Kumarb, and R. Samiyappan. 2007. PGPR-induced defense responses in the tea plant against blister blight disease. Crop Prot. 26: 556-565 DOI ScienceOn
22	Murphy, J. F., G. W. Zehnder, D. J. Schuster, E. J. Sikora, J. E. Polston, and J. W. Kloepper. 2000. Plant growth-promoting rhizobacterial mediated protection in tomato against tomato mottle virus. Plant Dis. 84: 779-784 DOI ScienceOn
23	Park, K. S. and J. W. Kloepper. 2000. Activation of PR-1a promoter by rhizobacteria that induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci. Biol. Control 18: 2-9 DOI ScienceOn
24	Xie, D. X., B. F. Feys, S. James, M. Nieto-Rostro, and J. G. Turner. 1998. Coi1: An Arabidopsis gene required for jasmonateregulated defense and fertility. Science 280: 1091-1094 DOI PUBMED ScienceOn
25	Emmert, E. A. B. and J. Handelsman. 1999. Biocontrol of plant disease: A Gram-positive perspective. FEMS Microbiol. Lett. 171: 1-9 DOI ScienceOn
26	Van Loon, L. C., P. A. H. M. Bakker, and M. J. Pieterse. 1998. Systemic induced resistance by rhizosphere bacteria. Annu. Rev. Phytopathol. 36: 453-483 DOI ScienceOn
27	Idris, E. E. S., O. Makarewicz, A. Farouk, K. Rosner, R. Greiner, H. Bochow, T. Richter, and R. Borriss. 2002. Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148: 2097-2109 PUBMED ScienceOn
28	Murphy, J. F., M. S. Reddy, C. M. Ryu, J. W. Kloepper, and R. Li. 2003. Rhizobacteria-mediated growth promotion of tomato leads to protection against cucumber mosaic virus. Phytopathology 93: 1301-1307 DOI ScienceOn
29	Peng, J. L., H. S. Dong, H. P. Dong, T. P. Delaney, B. M. Bonasera, and S. V. Beer. 2003. Harpin-elicited hypersensitive cell death and pathogen resistance requires the NDR1 and EDS1 genes. Physiol. Mol. Plant Pathol. 62: 317-326 DOI ScienceOn
30	Kessmann, H., T. Staub, J. Ligon, M. Oostendorp, and J. Ryals. 1994. Activation of systemic acquired disease resistance in plants. Eur. J. Plant Pathol. 100: 359-369 DOI ScienceOn
31	Pieterse, C. M. J., S. C. M. van Wees, E. Hoffland, J. A. van Pelt, and L. C. van Loon. 1996. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8: 1225-1237 DOI ScienceOn
32	Sticher, L., B. Mauch-Mani, and J. P. M $\acute{e}$ traux. 1997. Systemic acquired resistance. Annu. Rev. Phytopathol. 35: 235-270 DOI ScienceOn
33	Kloepper, J. W., M. S. Reddy, D. S. Kenney, C. Vavrina, N. Kokalis-Burelle, and N. Martinez-Ochoa. 2004. Theory and applications of rhizobacteria for transplant production and yield enhancement. Proc. XXVI IHC-Transplant Production and Stand Establishment. S. Nicola, J. Nowak, and C. S. Vavrina (eds.). Acta Hortic. 631: 219-229
34	Ryu, C. M., M. A. Farag, C. H. Hu, M. S. Reddy, H. X. Wei, P. W. Par $\acute{e}$ , and J. W. Kloepper. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100:4927-4932 DOI ScienceOn
35	Schneider, S. and W. R. Ullrich. 1991. Differential induction of resistance and enhanced enzyme activities in cucumber and tobacco caused by treatment with various abiotic and biotic inducers. Physiol. Mol. Plant Pathol. 45: 291-301 DOI ScienceOn
36	Kim, S. T., S. G. Kim, D. H. Hwang, S. Y. Kang, H. J. Kim, B. H. Lee, J. J. Lee, and K. Y. Kang. 2004. Proteomic analysis of pathogen-responsive proteins from rice leaves induced by rice blast fungus, Magnaporthe grisea. Proteomics 4: 3569-3578 DOI ScienceOn

Reference

3	(2009) Biocontrol science and technology Induction of systemic resistance in tobacco against<I>Tobacco mosaic virus</I>by<I>Bacillus</I>spp. / 21 (3) , 281
2	(2009) Journal of applied microbiology Biological control of anthracnose (<I>Colletotrichum gloeosporioides</I>) in yam by <I>Streptomyces</I> sp.MJM5763 / 111 (2) , 443
1	(2009) BioControl : journal of the International Organization for Biological Control 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 / 56 (1) , 113
1	(2012) Journal of plant interactions Response of barley to root colonization by<I>Pseudomonas</I>sp. DSMZ 13134 under laboratory, greenhouse, and field conditions / 7 (1) , 1
5	M. M. Elsharkawy. (2009) Plant pathology Induction of systemic resistance against <I>Cucumber mosaic virus</I> by <I>Penicillium simplicissimum</I> GP17‐2 in <I>Arabidopsis</I> and tobacco / 61 (5) , 964
1	Aurelien Bailly. (2012) Plant signaling & behavior The modulating effect of bacterial volatiles on plant growth : Current knowledge and future challenges / 7 (1) , 79
4	(2009) World journal of microbiology & biotechnology Isolation and characterisation of aerobic endospore forming Bacilli from sugarcane rhizosphere for the selection of strains with agriculture potentialities / 28 (4) , 1593
1	(2012) Plant and soil The plant growth-promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae induce systemic resistance against Cucumber mosaic virus in cucumber plants / 361 (1) , 397
4	(2012) MicrobiologyOpen Assessment of the relevance of the antibiotic 2-amino-3-(oxirane-2,3-dicarboxamido)-propanoyl-valine from <I>Pantoea agglomerans</I> biological control strains against bacterial plant pathogens / 1 (4) , 438
1	(2009) AMB Express Biotechnological potential of rhizobial metabolites to enhance the performance of <I>Bradyrhizobium</I> spp. and <I>Azospirillum brasilense</I> inoculants with soybean and maize / 3 (1) , 21
None	(2009) Frontiers in plant science Plant growth in <I>Arabidopsis</I> is assisted by compost soil-derived microbial communities / 4 (None) , 235
17	(2009) Proceedings of the National Academy of Sciences of the United States of America <I>Bacillus subtilis</I> biofilm induction by plant polysaccharides / 110 (17) , E1621
7	Mariangela Hungria. (2009) Biology and fertility of soils Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability / 49 (7) , 791
7	(2014) Molecular plant-microbe interactions : MPMI Plant Growth Promotion by Spermidine-Producing <I>Bacillus subtilis</I> OKB105 / 27 (7) , 655
1	(2009) AMB Express Identification and characterization of endophytic bacteria from corn ( <I>Zea mays</I> L.) roots with biotechnological potential in agriculture / 4 (1) , 26
None	(2009) BMC microbiology Transcriptome profiling of <I>Bacillus subtilis</I> OKB105 in response to rice seedlings / 15 (None) , 21
None	(2009) Frontiers in microbiology Biocontrol mechanism by root-associated <I>Bacillus amyloliquefaciens</I> FZB42 – a review / 6 (None) , 780
6	(2009) American journal of plant sciences Soybean Seed Co-Inoculation with &lt;i&gt;Bradyrhizobium&lt;/i&gt; spp. and &lt;i&gt;Azospirillum brasilense&lt;/i&gt;: A New Biotechnological Tool to Improve Yield and / 6 (6) , 811
49	(2009) African journal of microbiology research Enhanced plant growth and/or nitrogen fixation by leguminous and non-leguminous crops after single or dual inoculation of Streptomyces griseoflavus P4 with Bradyhizobium strains / 9 (49) , 2337
1	(2009) AMB Express Maize growth promotion by inoculation with <I>Azospirillum brasilense</I> and metabolites of <I>Rhizobium tropici</I> enriched on lipo-chitooligosaccharides (LCOs) / 5 (1) , 71
10	(2009) Plant disease Spraying of Leaf-Colonizing <I>Bacillus amyloliquefaciens</I> Protects Pepper from <I>Cucumber mosaic virus</I> / 100 (10) , 2099
1	Bishnu K. Shrestha. (2009) PLoS ONE Biological Control Activities of Rice-Associated <I>Bacillus</I> sp. Strains against Sheath Blight and Bacterial Panicle Blight of Rice / 11 (1) , e0146764
None	(2009) Frontiers in microbiology Plant Growth Promotion by Volatile Organic Compounds Produced by <I>Bacillus subtilis</I> SYST2 / 8 (None) , 171
None	(2009) Frontiers in microbiology Genome-Guided Insights into the Plant Growth Promotion Capabilities of the Physiologically Versatile <I>Bacillus aryabhattai</I> Strain AB211 / 8 (None) , 411
None	Ramalingam Radhakrishnan. (2009) Frontiers in physiology <I>Bacillus</I> : A Biological Tool for Crop Improvement through Bio-Molecular Changes in Adverse Environments / 8 (None) , 667
1	(2009) Agricultural sciences &lt;i&gt;Bacillus subtilis Strains&lt;/i&gt; with Antifungal Activity against the Phytopathogenic Fungi / 8 (1) , 1
4	(2009) Microbiology Volatile organic compounds produced by a soil-isolate, Bacillus subtilis FA26 induce adverse ultra-structural changes to the cells of Clavibacter michiganensis ssp. sepedonicus, the causal agent of ba / 163 (4) , 523
11	(2018) Functional plant biology : FPB Exogenous application of phenylacetic acid promotes root hair growth and induces the systemic resistance of tobacco against bacterial soft-rot pathogen Pectobacterium carotovorum subsp. carotovorum / 45 (11) , 1119
1	(2009) PLoS ONE Functional regions of HpaXm as elicitors with specific heat tolerance induce the hypersensitive response or plant growth promotion in nonhost plants / 13 (1) , e0188788
None	(2009) Scientific reports High temperatures affect the hypersensitive reaction, disease resistance and gene expression induced by a novel harpin HpaG-Xcm / 9 (None) , 990
None	(2009) Scientific reports Modulation of defence and iron homeostasis genes in rice roots by the diazotrophic endophyte Herbaspirillum seropedicae / 9 (None) , 10573
1	(2009) Symbiosis Halo-tolerant rhizospheric Arthrobacter woluwensis AK1 mitigates salt stress and induces physio-hormonal changes and expression of GmST1 and GmLAX3 in soybean / 77 (1) , 9
2	(2009) European journal of plant pathology Antagonistic potential of lipopeptide producing Bacillus amyloliquefaciens against major vegetable pathogens / 154 (2) , 319
3	(2009) European journal of plant pathology Control of Alternaria leaf spot of coriander in organic farming / 154 (3) , 575
12	(2009) Plants Mechanisms of Plant Tolerance to RNA Viruses Induced by Plant-Growth-Promoting Microorganisms / 8 (12) , 575
0	(2009) Brazilian archives of biology and technology Multiple Effect of Different Plant Growth Promoting Microorganisms on Beans (Phaseolus vulgaris L.) Crop / 63 (0) , e20190493
1	(2009) Applied biochemistry and microbiology Prospects and Applications of Lipopeptide-Producing Bacteria for Plant Protection (Review) / 56 (1) , 15
1	(2009) Applied biochemistry and microbiology Prospects and Applications of Lipopeptide-Producing Bacteria for Plant Protection (Review) / 56 (1) , 15
1	(2009) European journal of plant pathology Bacillus atrophaeus HAB-5 secretion metabolites preventing occurrence of systemic diseases in tobacco plant / 156 (1) , 159
9	(2009) Agronomy Bacillus velezensis PEA1 Inhibits Fusarium oxysporum Growth and Induces Systemic Resistance to Cucumber Mosaic Virus / 10 (9) , 1312
11	(2020) Pest management science Enhancing resistance of <I>Sesamum indicum</I> against <I>Alternaria sesami</I> through <I>Bacillus velezensis</I> AR1 / 76 (11) , 3577
None	(2009) The Science of the total environment Beneficial features of plant growth-promoting rhizobacteria for improving plant growth and health in challenging conditions: A methodical review / 743 (None) , 140682
6	(2009) Genomics Comparative transcriptomic analysis reveals that multiple hormone signal transduction and carbohydrate metabolic pathways are affected by <I>Bacillus cereus</I> in <I>Nicotiana tabacum</I> / 112 (6) , 4254
6	(2020) Applied biochemistry and microbiology Biological Methods of Plant Protection against Viruses: Problems and Prospects / 56 (6) , 624
11	(2009) Agronomy Endospore-Forming Bacteria Present in a Commercial Stabilized Poultry Manure Determines the Fusarium Biocontrol and the Tomato Growth Promotion / 10 (11) , 1636
None	(2009) BMC microbiology HpaXpm, a novel harpin of <I>Xanthomonas phaseoli</I> pv. <I>manihotis</I> , acts as an elicitor with high thermal stability, reduces disease, and promotes plant growth / 20 (None) , 4
20	(2009) Journal of plant nutrition Current scenario and future prospects of plant growth-promoting rhizobacteria: an economic valuable resource for the agriculture revival under stressful conditions / 43 (20) , 3062
None	(2009) Frontiers in genetics Draft Genome Sequence of Bacillus amyloliquefaciens Strain CB, a Biological Control Agent and Plant Growth-Promoting Bacterium Isolated From Cotton (Gossypium L.) Rhizosphere in Coimbatore, Tamil Nadu / 12 (None) , 704165
None	(2009) Frontiers in microbiology Diazotrophic Bacteria <I>Pantoea dispersa</I> and <I>Enterobacter asburiae</I> Promote Sugarcane Growth by Inducing Nitrogen Uptake and Defense-Related Gene Expression / 11 (None) , 600417
3	(2021) Microorganisms A Review on the Biotechnological Applications of the Operational Group Bacillus amyloliquefaciens / 9 (3) , 614
4	(2009) Pathogens Healthy Photosynthetic Mechanism Suggests ISR Elicited by Bacillus spp. in Capsicum chinense Plants Infected with PepGMV / 10 (4) , 455
None	(2009) Biological control : theory and applications in pest management Biological control of <I>Fusarium</I> wilt of sesame by <I>Penicillium bilaiae</I> 47M-1 / 158 (None) , 104601
8	(2009) Agronomy A Combined Nutrient/Biocontrol Agent Mixture Improve Cassava Tuber Yield and Cassava Mosaic Disease / 11 (8) , 1650
18	(2009) International journal of environmental research and public health Salt-Tolerant Compatible Microbial Inoculants Modulate Physio-Biochemical Responses Enhance Plant Growth, Zn Biofortification and Yield of Wheat Grown in Saline-Sodic Soil / 18 (18) , 9936
1	(2009) BMC genomics Antimicrobial activity screening of rhizosphere soil bacteria from tomato and genome-based analysis of their antimicrobial biosynthetic potential / 22 (1) , 29
1	(2009) Pest management science Mechanism of resistance to <I>Cucumber mosaic virus</I> elicited by inoculation with <I>Bacillus subtilis</I> subsp. <I>subtilis</I> / 78 (1) , 86
None	(2009) Journal of virological methods Flagellin and elongation factor of Bacillus velezensis (VB7) reprogramme the immune response in tomato towards the management of GBNV infection / 301 (None) , 114438