Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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The Endophytic Bacteria Bacillus velezensis Lle-9, Isolated from Lilium leucanthum, Harbors Antifungal Activity and Plant Growth-Promoting Effects

  • Khan, Mohammad Sayyar (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Gao, Junlian (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Chen, Xuqing (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Zhang, Mingfang (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Yang, Fengping (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Du, Yunpeng (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Moe, The Su (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Munir, Iqbal (Genomics and Bioinformatics Division, Institute of Biotechnology and Genetic Engineering (IBGE), The University of Agriculture) ;
  • Xue, Jing (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences) ;
  • Zhang, Xiuhai (Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry Sciences)
  • Received : 2019.10.13
  • Accepted : 2020.01.28
  • Published : 2020.05.28
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Abstract

Bacillus velezensis is an important plant growth-promoting rhizobacterium with immense potential in agriculture development. In the present study, Bacillus velezensis Lle-9 was isolated from the bulbs of Lilium leucanthum. The isolated strain showed antifungal activities against plant pathogens like Botryosphaeria dothidea, Fusarium oxysporum, Botrytis cinerea and Fusarium fujikuroi. The highest percentage of growth inhibition i.e., 68.56±2.35% was observed against Fusarium oxysporum followed by 63.12 ± 2.83%, 61.67 ± 3.39% and 55.82 ± 2.76% against Botrytis cinerea, Botryosphaeria dothidea, and Fusarium fujikuroi, respectively. The ethyl acetate fraction revealed a number of bioactive compounds and several were identified as antimicrobial agents such as diketopiperazines, cyclo-peptides, linear peptides, latrunculin A, 5α-hydroxy-6-ketocholesterol, (R)-S-lactoylglutathione, triamterene, rubiadin, moxifloxacin, 9-hydroxy-5Z,7E,11Z,14Z-eicosatetraenoic acid, D-erythro-C18-Sphingosine, citrinin, and 2-arachidonoyllysophosphatidylcholine. The presence of these antimicrobial compounds in the bacterial culture might have contributed to the antifungal activities of the isolated B. velezensis Lle-9. The strain showed plant growth-promoting traits such as production of organic acids, ACC deaminase, indole-3-acetic acid (IAA), siderophores, and nitrogen fixation and phosphate solubilization. IAA production was accelerated with application of exogenous tryptophan concentrations in the medium. Further, the lily plants upon inoculation with Lle-9 exhibited improved vegetative growth, more flowering shoots and longer roots than control plants under greenhouse condition. The isolated B. velezensis strain Lle-9 possessed broad-spectrum antifungal activities and multiple plant growth-promoting traits and thus may play an important role in promoting sustainable agriculture. This strain could be developed and applied in field experiments in order to promote plant growth and control disease pathogens.

Keywords

References

  1. Kloepper JW, Leong J, Teintze M, Schroth MN. 1980. Enhancing plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286: 885-886. https://doi.org/10.1038/286885a0
  2. Rodriguez H, Fraga R. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17: 319-339. https://doi.org/10.1016/S0734-9750(99)00014-2
  3. Glick BR, Cheng Z, Czarny J, Duan J. 2007. Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur. J. Plant Pathol. 119: 329-339. https://doi.org/10.1007/s10658-007-9162-4
  4. Velkov T, Thompson PE, Nation RL, Li J. 2010. Structure - activity relationships of polymyxin antibiotics. J. Med. Chem. 53: 1898-1916. https://doi.org/10.1021/jm900999h
  5. Kim YC, Leveau J, McSpadden Gardener BB, Pierson EA, Pierson LS, et al. 2011. The multifactorial basis for plant health promotion by plant-associated bacteria. Appl. Environ. Microbiol. 77: 1548-1555. https://doi.org/10.1128/AEM.01867-10
  6. Tendulkar SR, Saikumari YK, Patel V, Raghotama S, Munshi TK, Balaram P, et al. 2007. Isolation, purification and characterization of an antifungal molecule produced by Bacillus licheniformis BC98, and its effect on phytopathogen Magnaporthe grisea. Appl. Microbiol. 103: 2331-2339. https://doi.org/10.1111/j.1365-2672.2007.03501.x
  7. Wang J, Liu J, Chen H, Yao J. 2007. Characterization of Fusarium graminearum inhibitory lipopeptide from Bacillus subtilis IB. Appl. Microbiol. Biotechnol. 76: 889-894. https://doi.org/10.1007/s00253-007-1054-1
  8. Romero D, Perez-Garcia A, Rivera ME, Cazorla FM, de Vicente A. 2004. Isolation and evaluation of antagonistic bacteria towards the cucurbit powdery mildew fungus Podosphaera fusca. Appl. Microbiol. Biotechnol. 64: 263-269. https://doi.org/10.1007/s00253-003-1439-8
  9. Borriss R, Chen XH, Rueckert C, Blom J, Becker A, Baumgarth B, et al. 2011. Relationship of Bacillus amyloliquefaciens clades associated with strains DSM7T and FZB42T: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete genome sequence comparisons. Int. J. Syst. Evol. Microbiol. 61: 1786-1801. https://doi.org/10.1099/ijs.0.023267-0
  10. Perez-Garcia A, Romero D, de Vicente A. 2011. Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotechnol. 22: 187-193. https://doi.org/10.1016/j.copbio.2010.12.003
  11. Wang LT, Lee FL, Tai CJ, Kuo HP. 2008. Bacillus velezensis is a later heterotypic synonym of Bacillus amyloliquefaciens. Int. J. Syst. Evol. Microbiol. 58: 671-675. https://doi.org/10.1099/ijs.0.65191-0
  12. Dunlap CA, Kim SJ, Kwon SW, Rooney AP. 2015. Phylogenomic analysis shows that Bacillus amyloliquefaciens subsp. plantarum is a later heterotypic synonym of Bacillus methylotrophicus. Int. J. Syst. Evol. Microbiol. 65: 2104-2109. https://doi.org/10.1099/ijs.0.000226
  13. Madhaiyan M, Poonguzhali S, Kwon SW, Sa TM. 2010. Bacillus methylotrophicus sp. nov, a methanol-utilizing, plant-growthpromoting bacterium isolated from rice rhizosphere soil. Int. J. Syst. Evol. Microbiol. 60: 2490-2495. https://doi.org/10.1099/ijs.0.015487-0
  14. Chowdhury SP, Dietel K, Randler M, Schmid M, Junge H, Borriss R. et al. 2013. Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLoS One 8: e68818. https://doi.org/10.1371/journal.pone.0068818
  15. Chowdhury SP, Hartmann A, Gao X, Borriss R. 2015. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42-a review. Front. Microbiol. 6: 780.
  16. Rong LP, Lei JJ, Wang C. 2011. Collection and evaluation of the genus Lilium resources in Northeast China. Genet. Resour. Crop Evol. 58: 115-123. https://doi.org/10.1007/s10722-010-9584-2
  17. Chau CF, Wu SH. 2006. The development of regulations of Chinese herbal medicines for both medicinal and food uses. Trends Food Sci. Technol. 17: 313-323. https://doi.org/10.1016/j.tifs.2005.12.005
  18. You X, Xie C, Liu K, Gu Z. 2010. Isolation of non-starch polysaccharides from bulb of tiger lily (Lilium lancifolium Thunb) with fermentation of Saccharomyces cerevisiae. Carbohydr. Polym. 81: 35-40. https://doi.org/10.1016/j.carbpol.2010.01.051
  19. Schulz B, Boyle C, Draeger S, Rommert AK, Krohn K. 2002. Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol. Res. 106: 996-1004. https://doi.org/10.1017/S0953756202006342
  20. Tan RX, Zou WX. 2001. Endophytes: a rich source of functional metabolites. Nat. Prod. Rep. 18: 448-459. https://doi.org/10.1039/b100918o
  21. Strobel GA, Sears J, Kramer R, Sidhu RS, Hess WM. 1996. Taxol from Pestalotiopsis microspora an endophytic fungus of Taxus wallachiana. Microbiology 142: 435-440. https://doi.org/10.1099/13500872-142-2-435
  22. Vincent JM, Humphrey B. 1970. Taxonomically significant group antigens in Rhizobium. J. Gen. Microbiol. 63: 379-382. https://doi.org/10.1099/00221287-63-3-379
  23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739. https://doi.org/10.1093/molbev/msr121
  24. Khamna S, Yokota A, Lumyong S. 2009. Actinomycetes isolated from medicinal plant rhizospheric soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World J. Microbiol. Biotechnol. 25: 649-655. https://doi.org/10.1007/s11274-008-9933-x
  25. Lee S, Oh DG, Lee S, Kim G, Lee J, Son Y, et al. 2015. Chemotaxonomic metabolite profiling of 62 indigenous plant species and its correlation with bioactivities. Molecules 20: 19719-19734. https://doi.org/10.3390/molecules201119652
  26. Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, et al. 2016. Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat. Biotechnol. 34: 828-837. https://doi.org/10.1038/nbt.3597
  27. Chambers MC, Maclean B, Burke R, Amodei D, Ruderman DL, Neumann S, et al. 2012. A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 30: 918-920. https://doi.org/10.1038/nbt.2377
  28. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, et al. 2005. Cadmium-tolerant plant growthpromoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil. Biol. Biochem. 37: 241-250. https://doi.org/10.1016/j.soilbio.2004.07.033
  29. Truyens S, Jambon I, Croes S, Janssen J, Weyens N, Mench M, et al. 2014. The effect of long-term cd and ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. Int. J. Phytorem. 16: 643-659. https://doi.org/10.1080/15226514.2013.837027
  30. Cunningham JE, Kuiack C. 1992. Production of citric and oxalic acids and solubilization of calcium-phosphate by Penicillium bilaii. Appl. Environ. Microbiol. 58: 1451-1458. https://doi.org/10.1128/aem.58.5.1451-1458.1992
  31. Gordon SA, Weber RP. 1951. Colorimetric estimation of indoleacetic acid. Plant. Physiol. 26: 192-195. https://doi.org/10.1104/pp.26.1.192
  32. Schwyn B, Neilands JB. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56. https://doi.org/10.1016/0003-2697(87)90612-9
  33. Doebereiner J. 1994. Isolation and identification of aerobic nitrogen fixing bacteria. In: Alef K, Nannipieri P, pp. 134-141 (eds.), Methods in Applied Soil Microbiology and Biochemistry. Cambridge, MA, USA, Academic.
  34. Bashan Y, Holguin G, Lifshitz R. 1993. Isolation and characterization of plant growth-promoting rhizobacteria. In: Glick BR, Thompson JE, pp. 331-345 (eds.), Methods in Plant Molecular Biology and Biotechnology. BocaRaton, FL, USA, CRC Press.
  35. Mehta S, Nautiyal CS. 2001. An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr. Microbiol. 43: 51-56. https://doi.org/10.1007/s002840010259
  36. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, et al. 2007. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat. Biotechnol. 25: 1007-1014. https://doi.org/10.1038/nbt1325
  37. Rabbee MF, Ali MD, Choi J, Hwang BS, Jeong SC, Baek KH. 2019. Bacillus velezensis: A valuable member of bioactive molecules within plant microbiomes. Molecules 24: 1046. https://doi.org/10.3390/molecules24061046
  38. Yao A, Dr HB, Karimov S, Boturov U, Sanginboy S, Sharipov AK. 2006. Effect of FZB $24^{(R)}$ Bacillus subtilis as a biofertilizer on cotton yields in field tests. Arch. Phytopathol. Plant. Protect. 39: 323-328. https://doi.org/10.1080/03235400600655347
  39. Cai XC, Liua CH, Wang BT, Xuea YR. 2016. Genomic and metabolic traits endow Bacillus velezensis CC09 with a potential biocontrol agent in control of wheat powdery mildew disease. Microbiol. Res. 196: 89-94. https://doi.org/10.1016/j.micres.2016.12.007
  40. Zhang Y, Gao X, Wang S, Zhu C, Li R, Shen Q. 2018. Application of Bacillus velezensis NJAU-Z9 enhanced plant growth associated with efficient rhizospheric colonization monitored by qpcr with primers designed from the whole genome sequence. Curr. Microbiol. 75: 1574-1583. https://doi.org/10.1007/s00284-018-1563-4
  41. Horst RK. 2013. Field manual of diseases on fruits and vegetables. Springer Science+Business Media Dordrecht.
  42. Syed-Ab-Rahman SF, Carvalhais LC, Chua E, Xiao Y, Wass TJ, Schenk PM. 2018. Identification of soil bacterial isolates suppressing different Phytophthora spp. and promoting plant growth. Front. Plant. Sci. 9: 1502. https://doi.org/10.3389/fpls.2018.01502
  43. Martinez-Luis S, Ballesteros J, Gutierrez M. 2011. Antibacterial constituents from the octocoral-associated bacterium Pseudoalteromonas sp. Revista Latinoamericana Quimica. 39: 75-83.
  44. Nishanth Kumar S, Mohandas C, Siji J, Rajasekharan K, Nambisan B. 2012. Identification of antimicrobial compound, diketopiperazines, from a Bacillus sp. N strain associated with a rhabditid entomopathogenic nematode against major plant pathogenic fungi. J. Appl. Microbiol. 113: 914-924. https://doi.org/10.1111/j.1365-2672.2012.05385.x
  45. Yang E, Chang H. 2010. Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int. J. Food. Microbiol. 139: 56-63. https://doi.org/10.1016/j.ijfoodmicro.2010.02.012
  46. Wang XM, Bai YJ, Cai YJ, Zheng XH. 2017. Biochemical characteristics of three feruloyl esterases with a broad substrate spectrum from Bacillus amyloliquefaciens H47. Process. Biochem. 53: 109-115. https://doi.org/10.1016/j.procbio.2016.12.012
  47. Gill K, Kumar S, Xess I, Dey S. 2015. Novel synthetic anti-fungal tripeptide effective against Candida krusei. Ind. J. Med. Microbiol. 33: 110-116. https://doi.org/10.4103/0255-0857.148404
  48. Kloepper JW, Leong J, Teintze M, Schroth MN. 1980. Enhancing plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286: 885-886. https://doi.org/10.1038/286885a0
  49. Rao MRK, Philip S, Kumar MH, Saranya Y, Divya D, Prabhu K. 2015. GC-MS analysis, antimicrobial, antioxidant activity of an Ayurvedic medicine, Salmali Niryasa. J. Chem. Pharma. Res. 7: 131-139.
  50. Ismail NH, Ali AM, Aimi N, Kitajima M, Takayama H, Lajis NH. 1997. Anthraquinones from Morinda elliptica. Phytochemistry 45: 1723-1725. https://doi.org/10.1016/S0031-9422(97)00252-5
  51. Ali AM, Ismail NH, Mackeen MM, Yazan LS, Mohamed SM, Ho ASH, et al. 2000. Antiviral, cyototoxic and antimicrobial activities of anthraquinones isolated from the roots of Morinda elliptica. Pharma. Biol. 38: 298-301. https://doi.org/10.1076/1388-0209(200009)3841-AFT298
  52. Marioni J, da Silva MA, Cabreraa JL, Nunez Montoyaa SC, Paraje MG. 2016. The anthraquinones rubiadin and its 1-methyl ether isolated from Heterophyllaea pustulata reduces Candida tropicalis biofilms formation. Phytomedicine 23: 1321-1328. https://doi.org/10.1016/j.phymed.2016.07.008
  53. Matoba AY. 2012. Fungal keratitis responsive to Moxifloxacin monotherapy. Cornea 31: 1206-1209. https://doi.org/10.1097/ICO.0b013e31823f766c
  54. Lopes R, Tsui S, Goncalves PJRO, de Queirozm MV. 2018. A look into a multifunctional toolbox: endophytic Bacillus species provide broad and underexploited benefits for plants. World. J. Microbiol. Biotechnol. 34: 94. https://doi.org/10.1007/s11274-018-2479-7
  55. de Werra P, Pechy-Tarr M, Keel C, Maurhofer M. 2009. Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Appl. Environ. Microbiol. 75: 4162-4174. https://doi.org/10.1128/AEM.00295-09
  56. Todorovic B, Glick BR. 2008. The interconversion of ACC deaminase and D-cysteine desulfhydrase by directed mutagenesis. Planta 229: 193-205. https://doi.org/10.1007/s00425-008-0820-3
  57. Abeles FB, Morgan PW, Saltveit Jr ME. 1992. Ethylene in plant biology, pp. 1-13. 2nd edn. San Diego, Academic Press.
  58. Farwell AJ, Vesely S, Nero V, Rodriguez H, McCormack K, Shah S, et al. 2007. Tolerance of transgenic canola plants (Brassica napus) amended with plant growth-promoting bacteria to flooding stress at a metal-contaminated field site. Environ. Pollut. 147: 540-545. https://doi.org/10.1016/j.envpol.2006.10.014
  59. Meng Q, Jiang H, Hao JJ. 2016. Effects of Bacillus velezensis strain BAC03 in promoting plant growth. Biol. Cont. 98: 18-26. https://doi.org/10.1016/j.biocontrol.2016.03.010
  60. Xu M, Sheng J, Chen L, Men Y, Gan L, Guo S, et al. 2014. Bacterial community compositions of tomato (Lycopersicum esculentum Mill.) seeds and plant growth promoting activity of ACC deaminase producing Bacillus subtilis (HYT-12-1) on tomato seedlings. World. J. Microbiol. Biotechnol. 30: 835-845. https://doi.org/10.1007/s11274-013-1486-y
  61. Patten CL, Blakney AJC, Coulson TJD. 2013. Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria. Crit. Rev. Microbiol. 39: 395-415. https://doi.org/10.3109/1040841X.2012.716819
  62. Idris EE, Iglesias DJ, Talon M, Borriss R. 2007. Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol. Plant. Microbe. Interact. 20: 619-626 https://doi.org/10.1094/MPMI-20-6-0619
  63. Chagas Junior Af, De Oliveira AG, De Oliveira LA, Dos Santos Gr, Chagas LFB, Lopes da Silva AL, Luz Costa J. 2015. Production of indole-3-acetic acid by bacillus isolated from different soils. Bulg. J. Agric. Sci. 21: 282-287.
  64. Raza W, Shen Q. 2010. Growth, Fe3 + reductase activity, and siderophore production by Paenibacillus polymyxa SQR-21 under differential iron conditions. Curr. Microbiol. 61: 390-5. https://doi.org/10.1007/s00284-010-9624-3
  65. Kesaulya H, Hasinu JV, Tuhumury GNC. 2018. Potential of Bacillus spp produces siderophores in suppressing the wilt disease of banana plants. IOP Conference Series: Earth Environ. Sci. 102(1): 012016. https://doi.org/10.1088/1755-1315/102/1/012016
  66. Ferreira CMH, Vilas-Boas A, Sousa CA, Soares HMVM, Soares EV. 2019. Comparison of five bacterial strains producing siderophores with ability to chelate iron under alkaline conditions. AMB Express 9: 78. https://doi.org/10.1186/s13568-019-0796-3
  67. Tailor AJ, Joshi BH. 2012. Characterization and optimization of siderophore production from Pseudomonas fluorescens strain isolated from sugarcane rhizosphere. J. Environ. Res. Dev. 6: 688-694.
  68. Kumar VS, Menon S, Agarwal H, Gopalakrishnan D. 2017. Characterization and optimization of bacterium isolated from soil samples for the production of siderophores. Resource-Efficient Technol. 3: 434-439. https://doi.org/10.1016/j.reffit.2017.04.004
  69. Zhao L, Xu Y, Sun R, Deng Z, Yang W, Wei G. 2011. Identification and characterization of the endophytic plant growth prompter Bacillus cereus strain mq23 isolated from Sophora alopecuroides root nodules. Braz. J. Microbiol. 42: 567-575. https://doi.org/10.1590/S1517-83822011000200022
  70. Shen FT, Yen JH, Liao CS, Chen WC, Chao YT. 2019. Screening of rice endophytic biofertilizers with fungicide tolerance and plant growth-promoting characteristics. Sustainability 11: 1133. https://doi.org/10.3390/su11041133
  71. Borriss R. 2011. "Use of plant-associated Bacillus strains as biofertilizers and biocontrol agents," in Bacteria in Agrobiology. In: Maheshwari DK, pp. 41-76 (ed.), Plant Growth Responses. Heidelberg, Springer.
  72. Compant S, Brader G, Muzammil S, Sessitsch A, Lebrihi A, Mathieu F. 2013. Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases. BioControl 58: 435-455. https://doi.org/10.1007/s10526-012-9479-6
  73. Bach E, Dos Santos Seger GD, De Carvalho Fernandes G, Lisboa BB, Passaglia LMP. 2016. Evaluation of biological control and rhizosphere competence of plant growth promoting bacteria. Appl. Soil. Ecol. 99: 141-149. https://doi.org/10.1016/j.apsoil.2015.11.002
  74. van Lenteren JC, Bolckmans K, Kohl J, Ravensberg WJ, Urbaneja A. 2018. Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63: 39-59. https://doi.org/10.1007/s10526-017-9801-4
  75. Fan B, Wang C, Song X, Ding X, Wu L, Wu H, et al. 2018. Bacillus velezensis FZB42 in 2018: the gram-positive model strain for plant growth promotion and biocontrol. Front. Microbiol. 9: 2491. https://doi.org/10.3389/fmicb.2018.02491

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