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Contribution of indole-3-acetic acid in the plant growth promotion by the rhizospheric strain Bacillus amyloliquefaciens SQR9

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An Erratum to this article was published on 08 January 2015

Abstract

Bacillus amyloliquefaciens SQR9, isolated from the rhizosphere of cucumber, can control Fusarium wilt of cucumber and directly stimulate plant growth. To evaluate its potential agricultural use, the plant growth promotion of B. amyloliquefaciens SQR9 was evaluated, and the relative mechanisms, especially the production of the phytohormone indole-3-acetic acid (IAA), were investigated. The related plant-growth-promoting factors were genetically and chemically analyzed, and a mutant library was constructed for selecting strains with different IAA production. B. amyloliquefaciens SQR9 showed a growth-promoting activity in greenhouse experiments. Plant-growth-promoting factors like extracellular phytase, volatile components including acetoin, 2,3-butanediol, and phytohormone IAA were detected in B. amyloliquefaciens SQR9 cultures grown under laboratory conditions. Three IAA production mutant strains showed variation in plant-growth-promoting effect. IAA production in B. amyloliquefaciens SQR9 was related to its plant-growth-promoting effect, but IAA alone could not account for the overall observed plant-growth-promoting effect. The promoted plant growth by the rhizospheric strain B. amyloliquefaciens SQR9 can be attributed to multiple factors, including production of phytohormones, volatile compounds, and extracellular enzymes. Therefore, the strain B. amyloliquefaciens SQR9 may be used as a plant-growth-promoting agent to increase crop yield.

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References

  • Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886

    Article  CAS  PubMed  Google Scholar 

  • Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570

    Article  CAS  PubMed  Google Scholar 

  • Barbieri P, Galli E (1993) Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production. Res Microbiol 144:69–75

    Article  CAS  PubMed  Google Scholar 

  • Bashan Y, Holguin G, De-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577

    Article  CAS  PubMed  Google Scholar 

  • Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503

    Article  CAS  PubMed  Google Scholar 

  • Brandl MT, Lindow SE (1997) Environmental signals modulate the expression of an indole-3-acetic acid biosynthetic gene in Erwinia herbicola. Mol Plant Microbe Interact 10:499–505

    Article  CAS  Google Scholar 

  • Breton YL, Mohapatra NP, Haldenwang WG (2006) In vivo random mutagenesis of Bacillus subtilis by use of TnYLB-1, a mariner-based transposon. Appl Environ Microbiol 72:327–333

    Article  PubMed Central  PubMed  Google Scholar 

  • Cao Y, Zhang Z, Ling N, Yuan Y, Zheng X, Shen B, Shen Q (2011) Bacillus subtilis SQR 9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol Fertil Soils 47:495–506

    Article  CAS  Google Scholar 

  • Chaiharn M, Lumyong S (2011) Screening and optimization of indole-3-acetic acid production and phosphate solubilization from rhizobacteria aimed at improving plant growth. Curr Microbiol 62:173–181

    Article  CAS  PubMed  Google Scholar 

  • Duca D, Lorv J, Patten CL, Rose D, Glick BR (2013) Indole-3-acetic acid in plant–microbe interactions. Antonie Van Leeuwenhoek 1–41

  • Emmert EA, Handelsman J (1999) Biocontrol of plant disease: a gram-positive perspective. FEMS Microbiol Lett 171:1–9

    Article  CAS  PubMed  Google Scholar 

  • Farag MA, Paré PW (2002) C6-Green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554

    Article  CAS  PubMed  Google Scholar 

  • Farag MA, Ryu CM, Sumner LW, Paré 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

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE (2001) Surface-to-air signals. Nature 411:854–856

    Article  CAS  PubMed  Google Scholar 

  • Frommel MI, Nowak J, Lazarovits G (1991) Growth enhancement and developmental modifications of in vitro grown potato (solanumtuberosum spp. tuberosum) as affected by a nonfluorescent pseudomonas sp. Plant Physiol 96:928–936

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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. J Plant Dis Prot 111:583–597

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Nakaya A (2002) The KEGG databases at GenomeNet. Nucleic Acids Res 30:42–46

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kerovuo J, Lauraeus M, Nurminen P, Kalkkinen N, Apajalahti J (1998) Isolation, characterization, molecular gene cloning, and sequencing of a novel phytase from Bacillus subtilis. Appl Environ Microbiol 64:2079–2085

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kim YO, Lee JK, Kim HK, Yu JH, Oh TK (1998) Cloning of the thermostable phytase gene (phy) from Bacillus sp. DS11 and its overexpression in Escherichia coli. FEMS Microbiol Lett 162:185–191

    Article  CAS  PubMed  Google Scholar 

  • Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–44

    Article  Google Scholar 

  • Koburger T, Weibezahn J, Bernhardt J, Homuth G, Hecker M (2005) Genome-wide mRNA profiling in glucose starved Bacillus subtilis cells. Mol Genet Genomics 274:1–12

    Article  CAS  PubMed  Google Scholar 

  • Kochar M, Upadhyay A, Srivastava S (2011) Indole-3-acetic acid biosynthesis in the biocontrol strain Pseudomonas fluorescens Psd and plant growth regulation by hormone overexpression. Res Microbiol 162:426–435

    Article  CAS  PubMed  Google Scholar 

  • Kuras R, Saint-Marcoux D, Wollman FA, Vitry CD (2007) A specific c-type cytochrome maturation system is required for oxygenic photosynthesis. Proc Natl Acad Sci 104:9906–9910

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Landy M, Warren GH, Rosenman SB, Colio LG (1948) Bacillomycin an antibiotic from Bacillus subtilis active against pathogenic Fungi. Exp Biol Med 67:539–541

    Article  CAS  Google Scholar 

  • Liu Y, Shi J, Feng Y, Yang X, Li X, Shen Q (2013) Tobacco bacterial wilt can be biologically controlled by the application of antagonistic strains in combination with organic fertilizer. Biol Fertil Soils 49:447–464

    Article  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Ryu J, Sa T (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278

    Article  CAS  PubMed  Google Scholar 

  • Makarewicz O, Dubrac S, Msadek T, Borriss R (2006) Dual role of the Pho∼P approximately P response regulator: Bacillus amyloliquefaciens FZB45 phytase gene transcription is directed by positive and negative interactions with the phyC promoter. J Bacteriol 188(19):6953–65

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Meyer JR, Linderman RG (1986) Selective influence on populations of rhizosphere or rhizoplane bacteria and actinomycetes by mycorrhizas formed by Glomus fasciculatum. Soil Biol Biochem 18:191–196

    Article  Google Scholar 

  • Nicholson WL (2008) The Bacillus subtilis ydjL (bdhA) gene encodes acetoin reductase/2,3-butanediol dehydrogenase. Appl Environ Microbiol 74:6832–6838

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Palacios OA, Bashan Y, De-Bashan LE (2014) Proven and potential involvement of vitamins in interactions of plants with plant growth-promoting bacteria—an overview. Biol Fertil Soils 50:415–432

    Article  CAS  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Penrose DM, Glick BR (2001) Levels of ACC and related compounds in exudate and extracts of canola seeds treated with ACC deaminase-containing plant growth-promoting bacteria. Can J Microbiol 47:368–372

    Article  CAS  PubMed  Google Scholar 

  • Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266

    Article  CAS  PubMed  Google Scholar 

  • Qiu M, Li S, Zhou X, Cui X, Vivanco JM, Zhang N, Shen Q, Zhang R (2014) De-coupling of root–microbiome associations followed by antagonist inoculation improves rhizosphere soil suppressiveness. Biol Fertil Soils 50:217–224

    Article  CAS  Google Scholar 

  • Qiu M, Zhang R, Xue C, Zhang S, Li S, Zhang N, Shen Q (2012) Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fertil Soils 48:807–816

    Article  CAS  Google Scholar 

  • Renna MC, Najimudin N, Winik LR, Zahler SA (1993) Regulation of the Bacillus subtilis alsS, alsD, and alsR genes involved in post-exponential-phase production of acetoin. J Bacteriol 175:3863–3875

    PubMed Central  CAS  PubMed  Google Scholar 

  • Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649

    Article  CAS  PubMed  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pw P (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Wei HX, Paré PW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Santana M, Kunst F, Hullo MF, Rapoport G, Danchin A, Glaser P (1992) Molecular cloning, sequencing, and physiological characterization of the qox operon from Bacillus subtilis encoding the aa3-600 quinol oxidase. J Biol Chem 267:10225–10231

    CAS  PubMed  Google Scholar 

  • Shimizu M (1992) Purification and characterization of phytase from Bacillus subtilis (natto) N-77. Biosci Biotech Bioch 56:1266–1269

    Article  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    Article  CAS  PubMed  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, Ruan Y, Shen Q (2013) Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49:435–446

    Article  Google Scholar 

  • Weng J, Wang Y, Li J, Shen Q, Zhang R (2013) Enhanced root colonization and biocontrol activity of Bacillus amyloliquefaciens SQR9 by abrB gene disruption. Appl Microbiol Biotechnol 97:8823–8830

    Article  CAS  PubMed  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu Z, Shao J, Li B, Yan X, Shen Q, Zhang R (2013) Contribution of bacillomycin D in Bacillus amyloliquefaciens SQR9 to antifungal activity and biofilm formation. Appl Environ Microbiol 79:808–815

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was financially supported by the Chinese Ministry of Science and Technology (2013AA102802 and 2011BAD11B03). NZ was supported by the Fundamental Research Funds for the Central Universities (KYZ201408); RZ and QS were also supported by the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions and the 111 Project (B12009).

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Authors and Affiliations

  1. National Engineering Research Center for Organic-based Fertilizers, and Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Jiahui Shao, Zhihui Xu, Nan Zhang, Qirong Shen & Ruifu Zhang

  2. Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, People’s Republic of China

    Ruifu Zhang

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  1. Jiahui Shao
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  2. Zhihui Xu
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  3. Nan Zhang
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  5. Ruifu Zhang
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Correspondence to Ruifu Zhang.

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Shao, J., Xu, Z., Zhang, N. et al. Contribution of indole-3-acetic acid in the plant growth promotion by the rhizospheric strain Bacillus amyloliquefaciens SQR9. Biol Fertil Soils 51, 321–330 (2015). https://doi.org/10.1007/s00374-014-0978-8

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