Journal of Microbiology and Biotechnology

  • 제19권10호
  • /
  • Pages.1250-1258
  • /
  • 2009
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

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)
  • 발행 : 2009.10.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

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.

키워드

참고문헌

  1. 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 https://doi.org/10.1016/S0092-8674(00)81858-9
  2. 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 https://doi.org/10.1105/tpc.011965
  3. 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 https://doi.org/10.1105/tpc.12.11.2175
  4. Dangl, J. L. and J. D. Jones. 2001. Plant pathogens and integrated defense responses to infection. Nature 411: 826-833 https://doi.org/10.1038/35081161
  5. Dobbelaere, S., J. Vanderleyden, and Y. Okon. 2003. Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit. Rev. Plant Sci. 22: 107-149 https://doi.org/10.1080/713610853
  6. Dong, X. 1998. SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1: 316-323 https://doi.org/10.1016/1369-5266(88)80053-0
  7. Emmert, E. A. B. and J. Handelsman. 1999. Biocontrol of plant disease: A Gram-positive perspective. FEMS Microbiol. Lett. 171: 1-9 https://doi.org/10.1111/j.1574-6968.1999.tb13405.x
  8. 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
  9. 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
  10. 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 https://doi.org/10.1007/BF01874804
  11. 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 https://doi.org/10.1002/pmic.200400999
  12. 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 https://doi.org/10.1094/PHYTO.2004.94.11.1259
  13. 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
  14. 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
  15. 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 https://doi.org/10.1094/PHYTO.2003.93.10.1292
  16. 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
  17. 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
  18. 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 https://doi.org/10.1094/Phyto-84-139
  19. Mou, Z., W. Fan, and X. Dong. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 815-826 https://doi.org/10.1016/S0092-8674(03)00473-2
  20. 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 https://doi.org/10.1094/PHYTO.2003.93.10.1301
  21. 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 https://doi.org/10.1094/PDIS.2000.84.7.779
  22. 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 https://doi.org/10.1006/bcon.2000.0815
  23. 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 https://doi.org/10.1016/S0885-5765(03)00078-X
  24. 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 https://doi.org/10.1105/tpc.8.8.1225
  25. 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 https://doi.org/10.1105/tpc.10.9.1571
  26. 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 https://doi.org/10.1073/pnas.0730845100
  27. 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
  28. 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 https://doi.org/10.1016/j.cropro.2006.05.007
  29. 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
  30. 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 https://doi.org/10.1016/S0885-5765(05)80060-8
  31. Sticher, L., B. Mauch-Mani, and J. P. M$\acute{e}$traux. 1997. Systemic acquired resistance. Annu. Rev. Phytopathol. 35: 235-270 https://doi.org/10.1146/annurev.phyto.35.1.235
  32. 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 https://doi.org/10.1146/annurev.phyto.36.1.453
  33. 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 https://doi.org/10.1094/MPMI-18-0385
  34. 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 https://doi.org/10.1126/science.280.5366.1091
  35. 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 https://doi.org/10.1023/A:1009923702103
  36. 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 https://doi.org/10.1023/B:PLSO.0000037048.26437.fa

피인용 문헌

  1. Induction of systemic resistance in tobacco againstTobacco mosaic virusbyBacillusspp. vol.21, pp.3, 2009, https://doi.org/10.1080/09583157.2010.543667
  2. Biological control of anthracnose (Colletotrichum gloeosporioides) in yam by Streptomyces sp.MJM5763 vol.111, pp.2, 2009, https://doi.org/10.1111/j.1365-2672.2011.05048.x
  3. 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 vol.56, pp.1, 2009, https://doi.org/10.1007/s10526-010-9306-x
  4. Response of barley to root colonization byPseudomonassp. DSMZ 13134 under laboratory, greenhouse, and field conditions vol.7, pp.1, 2012, https://doi.org/10.1080/17429145.2011.597002
  5. Induction of systemic resistance against Cucumber mosaic virus by Penicillium simplicissimum GP17‐2 in Arabidopsis and tobacco vol.61, pp.5, 2009, https://doi.org/10.1111/j.1365-3059.2011.02573.x
  6. The modulating effect of bacterial volatiles on plant growth : Current knowledge and future challenges vol.7, pp.1, 2012, https://doi.org/10.4161/psb.7.1.18418
  7. Isolation and characterisation of aerobic endospore forming Bacilli from sugarcane rhizosphere for the selection of strains with agriculture potentialities vol.28, pp.4, 2009, https://doi.org/10.1007/s11274-011-0965-2
  8. The plant growth-promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae induce systemic resistance against Cucumber mosaic virus in cucumber plants vol.361, pp.1, 2012, https://doi.org/10.1007/s11104-012-1255-y
  9. Assessment of the relevance of the antibiotic 2-amino-3-(oxirane-2,3-dicarboxamido)-propanoyl-valine from Pantoea agglomerans biological control strains against bacterial plant pathogens vol.1, pp.4, 2012, https://doi.org/10.1002/mbo3.43
  10. Biotechnological potential of rhizobial metabolites to enhance the performance of Bradyrhizobium spp. and Azospirillum brasilense inoculants with soybean and maize vol.3, pp.1, 2009, https://doi.org/10.1186/2191-0855-3-21
  11. Plant growth in Arabidopsis is assisted by compost soil-derived microbial communities vol.4, pp.None, 2009, https://doi.org/10.3389/fpls.2013.00235
  12. Bacillus subtilis biofilm induction by plant polysaccharides vol.110, pp.17, 2009, https://doi.org/10.1073/pnas.1218984110
  13. Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability vol.49, pp.7, 2009, https://doi.org/10.1007/s00374-012-0771-5
  14. Plant Growth Promotion by Spermidine-Producing Bacillus subtilis OKB105 vol.27, pp.7, 2014, https://doi.org/10.1094/mpmi-01-14-0010-r
  15. Identification and characterization of endophytic bacteria from corn ( Zea mays L.) roots with biotechnological potential in agriculture vol.4, pp.1, 2009, https://doi.org/10.1186/s13568-014-0026-y
  16. Transcriptome profiling of Bacillus subtilis OKB105 in response to rice seedlings vol.15, pp.None, 2009, https://doi.org/10.1186/s12866-015-0353-4
  17. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review vol.6, pp.None, 2009, https://doi.org/10.3389/fmicb.2015.00780
  18. Soybean Seed Co-Inoculation with <i>Bradyrhizobium</i> spp. and <i>Azospirillum brasilense</i>: A New Biotechnological Tool to Improve Yield and vol.6, pp.6, 2009, https://doi.org/10.4236/ajps.2015.66087
  19. 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 vol.9, pp.49, 2009, https://doi.org/10.5897/ajmr2015.7796
  20. Maize growth promotion by inoculation with Azospirillum brasilense and metabolites of Rhizobium tropici enriched on lipo-chitooligosaccharides (LCOs) vol.5, pp.1, 2009, https://doi.org/10.1186/s13568-015-0154-z
  21. Spraying of Leaf-Colonizing Bacillus amyloliquefaciens Protects Pepper from Cucumber mosaic virus vol.100, pp.10, 2009, https://doi.org/10.1094/pdis-03-16-0314-re
  22. Biological Control Activities of Rice-Associated Bacillus sp. Strains against Sheath Blight and Bacterial Panicle Blight of Rice vol.11, pp.1, 2009, https://doi.org/10.1371/journal.pone.0146764
  23. Plant Growth Promotion by Volatile Organic Compounds Produced by Bacillus subtilis SYST2 vol.8, pp.None, 2009, https://doi.org/10.3389/fmicb.2017.00171
  24. Genome-Guided Insights into the Plant Growth Promotion Capabilities of the Physiologically Versatile Bacillus aryabhattai Strain AB211 vol.8, pp.None, 2009, https://doi.org/10.3389/fmicb.2017.00411
  25. Bacillus : A Biological Tool for Crop Improvement through Bio-Molecular Changes in Adverse Environments vol.8, pp.None, 2009, https://doi.org/10.3389/fphys.2017.00667
  26. <i>Bacillus subtilis Strains</i> with Antifungal Activity against the Phytopathogenic Fungi vol.8, pp.1, 2009, https://doi.org/10.4236/as.2017.81001
  27. 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 vol.163, pp.4, 2009, https://doi.org/10.1099/mic.0.000451
  28. 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 vol.45, pp.11, 2018, https://doi.org/10.1071/fp17332
  29. Functional regions of HpaXm as elicitors with specific heat tolerance induce the hypersensitive response or plant growth promotion in nonhost plants vol.13, pp.1, 2009, https://doi.org/10.1371/journal.pone.0188788
  30. High temperatures affect the hypersensitive reaction, disease resistance and gene expression induced by a novel harpin HpaG-Xcm vol.9, pp.None, 2009, https://doi.org/10.1038/s41598-018-37886-9
  31. Modulation of defence and iron homeostasis genes in rice roots by the diazotrophic endophyte Herbaspirillum seropedicae vol.9, pp.None, 2009, https://doi.org/10.1038/s41598-019-45866-w
  32. Halo-tolerant rhizospheric Arthrobacter woluwensis AK1 mitigates salt stress and induces physio-hormonal changes and expression of GmST1 and GmLAX3 in soybean vol.77, pp.1, 2009, https://doi.org/10.1007/s13199-018-0562-3
  33. Antagonistic potential of lipopeptide producing Bacillus amyloliquefaciens against major vegetable pathogens vol.154, pp.2, 2009, https://doi.org/10.1007/s10658-018-01658-y
  34. Control of Alternaria leaf spot of coriander in organic farming vol.154, pp.3, 2009, https://doi.org/10.1007/s10658-019-01682-6
  35. Mechanisms of Plant Tolerance to RNA Viruses Induced by Plant-Growth-Promoting Microorganisms vol.8, pp.12, 2009, https://doi.org/10.3390/plants8120575
  36. Multiple Effect of Different Plant Growth Promoting Microorganisms on Beans (Phaseolus vulgaris L.) Crop vol.63, pp.0, 2009, https://doi.org/10.1590/1678-4324-solo-2020190493
  37. Prospects and Applications of Lipopeptide-Producing Bacteria for Plant Protection (Review) vol.56, pp.1, 2009, https://doi.org/10.1134/s0003683820010135
  38. Prospects and Applications of Lipopeptide-Producing Bacteria for Plant Protection (Review) vol.56, pp.1, 2009, https://doi.org/10.1134/s0003683820010135
  39. Bacillus atrophaeus HAB-5 secretion metabolites preventing occurrence of systemic diseases in tobacco plant vol.156, pp.1, 2009, https://doi.org/10.1007/s10658-019-01873-1
  40. Bacillus velezensis PEA1 Inhibits Fusarium oxysporum Growth and Induces Systemic Resistance to Cucumber Mosaic Virus vol.10, pp.9, 2009, https://doi.org/10.3390/agronomy10091312
  41. Enhancing resistance of Sesamum indicum against Alternaria sesami through Bacillus velezensis AR1 vol.76, pp.11, 2020, https://doi.org/10.1002/ps.5890
  42. Beneficial features of plant growth-promoting rhizobacteria for improving plant growth and health in challenging conditions: A methodical review vol.743, pp.None, 2009, https://doi.org/10.1016/j.scitotenv.2020.140682
  43. Comparative transcriptomic analysis reveals that multiple hormone signal transduction and carbohydrate metabolic pathways are affected by Bacillus cereus in Nicotiana tabacum vol.112, pp.6, 2009, https://doi.org/10.1016/j.ygeno.2020.07.022
  44. Biological Methods of Plant Protection against Viruses: Problems and Prospects vol.56, pp.6, 2020, https://doi.org/10.1134/s0003683820060101
  45. Endospore-Forming Bacteria Present in a Commercial Stabilized Poultry Manure Determines the Fusarium Biocontrol and the Tomato Growth Promotion vol.10, pp.11, 2009, https://doi.org/10.3390/agronomy10111636
  46. HpaXpm, a novel harpin of Xanthomonas phaseoli pv. manihotis , acts as an elicitor with high thermal stability, reduces disease, and promotes plant growth vol.20, pp.None, 2009, https://doi.org/10.1186/s12866-019-1691-4
  47. Current scenario and future prospects of plant growth-promoting rhizobacteria: an economic valuable resource for the agriculture revival under stressful conditions vol.43, pp.20, 2009, https://doi.org/10.1080/01904167.2020.1799004
  48. 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 vol.12, pp.None, 2009, https://doi.org/10.3389/fgene.2021.704165
  49. Diazotrophic Bacteria Pantoea dispersa and Enterobacter asburiae Promote Sugarcane Growth by Inducing Nitrogen Uptake and Defense-Related Gene Expression vol.11, pp.None, 2009, https://doi.org/10.3389/fmicb.2020.600417
  50. A Review on the Biotechnological Applications of the Operational Group Bacillus amyloliquefaciens vol.9, pp.3, 2021, https://doi.org/10.3390/microorganisms9030614
  51. Healthy Photosynthetic Mechanism Suggests ISR Elicited by Bacillus spp. in Capsicum chinense Plants Infected with PepGMV vol.10, pp.4, 2009, https://doi.org/10.3390/pathogens10040455
  52. Biological control of Fusarium wilt of sesame by Penicillium bilaiae 47M-1 vol.158, pp.None, 2009, https://doi.org/10.1016/j.biocontrol.2021.104601
  53. A Combined Nutrient/Biocontrol Agent Mixture Improve Cassava Tuber Yield and Cassava Mosaic Disease vol.11, pp.8, 2009, https://doi.org/10.3390/agronomy11081650
  54. Salt-Tolerant Compatible Microbial Inoculants Modulate Physio-Biochemical Responses Enhance Plant Growth, Zn Biofortification and Yield of Wheat Grown in Saline-Sodic Soil vol.18, pp.18, 2009, https://doi.org/10.3390/ijerph18189936
  55. Antimicrobial activity screening of rhizosphere soil bacteria from tomato and genome-based analysis of their antimicrobial biosynthetic potential vol.22, pp.1, 2009, https://doi.org/10.1186/s12864-020-07346-8
  56. Mechanism of resistance to Cucumber mosaic virus elicited by inoculation with Bacillus subtilis subsp. subtilis vol.78, pp.1, 2009, https://doi.org/10.1002/ps.6610
  57. Flagellin and elongation factor of Bacillus velezensis (VB7) reprogramme the immune response in tomato towards the management of GBNV infection vol.301, pp.None, 2009, https://doi.org/10.1016/j.jviromet.2021.114438