Skip to main content
Log in

Bacillus amyloliquefaciens subsp. plantarum GR53, a potent biocontrol agent resists Rhizoctonia disease on Chinese cabbage through hormonal and antioxidants regulation

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The fungus Rhizoctonia solani is one of the causal agents of numerous diseases that affect crop growth and yield. The aim of this present investigation was to identify a biocontrol agent that acts against R. solani and to determine the agent’s protective effect through phytohormones and antioxidant regulation in experimentally infected Chinese cabbage plants. Four rhizospheric soil bacterial isolates GR53, GR169, GR786, and GR320 were tested for their antagonistic activity against R. solani. Among these isolates, GR53 significantly suppressed fungal growth. GR53 was identified as Bacillus amyloliquefaciens subsp. plantarum by phylogenetic analysis of the 16S rDNA sequence. The biocontrol activity of B. amyloliquefaciens subsp. plantarum GR53 was tested in Chinese cabbage plants under controlled conditions. Results showed that R. solani inhibited plant growth (length, width, fresh and dry weight of leaves) by reducing chlorophyll and total phenolic content, as well as by increasing the levels of salicylic acid, jasmonic acid, abscisic acid, and DPPH scavenging activity. By regulating the levels of these compounds, the co-inoculation of B. amyloliquefaciens subsp. plantarum GR53 heightened induced systemic resistance in infected Chinese cabbage, effectively mitigating R. solani-induced damaging effects and improving plant growth. The results obtained from this study suggest that B. amyloliquefaciens subsp. plantarum GR53 is an effective biocontrol agent to prevent the damage caused by R. solani in Chinese cabbage plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adachi M, Sako Y, Ishida Y (1996) Analysis of Alexandrium (Dinophyceae) species using sequences of the 5.8 S ribosomal DNA and internal transcribed spacer regions. J Phycol 32:424–432

    Article  CAS  Google Scholar 

  • Amerine MA, Ough CS (1980) Methods for analysis of musts and wine. Wiley, New York, pp 205–206

    Google Scholar 

  • Asaka O, Shoda M (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62:4081–4085

    CAS  Google Scholar 

  • Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  Google Scholar 

  • Benhamou N, Kloepper JW, Quadt-Hallman A, Tuzon S (1996) Induction of defense-related ultrastructural modification in pea root tissues inoculated with endophytic bacteria. Plant Physiol 112:919–929

    CAS  Google Scholar 

  • Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200

    Article  CAS  Google Scholar 

  • Buonaurio R, Scarponi L, Ferrara L, Sidoti P, Bertona A (2002) Induction of systemic acquired resistance in pepper by acibenzolar-S-methyl against bacterial spot disease. Eur J Plant Pathol 108:41–49

    Article  CAS  Google Scholar 

  • Chatterjee A, Ghosh SK (2008) Alterations in biochemical components in mesta plants infected with yellow vein mosaic disease. Braz J Plant Physiol 20:267–275

    Article  Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886

    Article  CAS  Google Scholar 

  • Choudhary DK (2011) Plant growth promotion (PGP) activities and molecular characterization of rhizobacterial strains isolated from soybean (Glycine max L. Merril) plants against charcoal rot pathogen, Macrophomina phaseolina. Biotechnol Lett 33:2287–2295

    Article  CAS  Google Scholar 

  • Chowdhury SP, Dietel K, Randler M, Schmid M, Junge H, Borriss R, Hartmann A, Grosch R (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

    Article  Google Scholar 

  • Chung SH, Kim SD (2005) Biological control of phytopathogenic fungi by Bacillus amyloliquefaciens 7079; suppression rates are better than popular chemical fungicides. J Microbiol Biotechnol 15:1011–1021

    CAS  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:49–51

    Google Scholar 

  • Correa OS, Montecchia MS, Berti MF, Ferrari MCF, Pucheu NL, Kerber NL, Garcia AF (2009) Bacillus amyloliquefaciens BNM122, a potential microbial biocontrol agent applied on soybean seeds, causes a minor impact on rhizosphere and soil microbial communities. Appl Soil Ecol 41:185–194

    Article  Google Scholar 

  • Dixon RA, Harrison MG (1992) Activation, structure and organization of genes involved in microbial defense in plants. Adv Genet 28:165–234

    Article  Google Scholar 

  • Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992) Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci USA 89:2480–2484

    Article  CAS  Google Scholar 

  • Gara LD, de-Pinto MC, Tommasi F (2003) The antioxidant systems vis-a-vis reactive oxygen species during plant–pathogen interaction. Plant Physiol Biochem 41:863–870

    Article  Google Scholar 

  • Gasoni L, Gurfinkel BSD (2009) Biocontrol of Rhizoctonia solani by the endophytic fungus Cladorrhinum foecundissimum in cotton plants. Australas J Plant Pathol 38:389–391

    Article  Google Scholar 

  • Gonzalez-Garcia V, Portal-Onco MA, Rubio-Susan V (2006) Review: biology and systematics of the form genus Rhizoctonia. Span J Agric Res 4:55–79

    Article  Google Scholar 

  • Hadar Y, Chet I, Henis Y (1979) Biological control of Rhizoctonia solani damping-off with wheat bran culture of Trichoderma harzianum. Phytopathology 69:64–68

    Article  CAS  Google Scholar 

  • He H, Silo-Suh LA, Handelsman J, Clardy J (1994) Zwittermicin A, an antifungal and plant protection agent from Bacillus cereus. Tetrahedron Lett 35:2499–2502

    Article  CAS  Google Scholar 

  • Huang X, Zhang N, Yong X, Yang X, Shen Q (2012) Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus SQR-N43. Microbiol Res 167:135–143

    Article  CAS  Google Scholar 

  • Ji SH, Paul NC, Deng JX, Kim YS, Yun BS, Yu SH (2013) Biocontrol activity of Bacillus amyloliquefaciens CNU114001 against fungal plant diseases. Mycobiology 41:234–242

    Article  CAS  Google Scholar 

  • Johnsen K, Jacobsen C, Torsvik V, Sorensen J (2001) Pesticide effects on bacterial diversity in agricultural soils—a review. Biol Fertil Soils 33:443–453

    Article  CAS  Google Scholar 

  • Kang SM, Radhakrishnan R, You YH, Joo GJ, Lee IJ (2014) Phosphate solubilizing Bacillus megaterium mj1212 regulates endogenous plant carbohydrates and amino acids contents to promote mustard plant growth. Indian J Microbiol 54:427–433

    Article  CAS  Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2006) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  Google Scholar 

  • Lee MK, Chun JH, Byeon DH, Chung SO, Park SU, Park S, Arasu MV, Al-Dhabif NA, Limg YP, Kim SJ (2014) Variation of glucosinolates in 62 varieties of Chinese cabbage (Brassica rapa L. ssp. pekinensis) and their antioxidant activity. LWT Food Sci Technol 58:93–101

    Article  CAS  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472

    Article  CAS  Google Scholar 

  • Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signaling network. Curr Opin Plant Biol 8:532–540

    Article  CAS  Google Scholar 

  • Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Curr Opin Plant Biol 8:409–414

    Article  CAS  Google Scholar 

  • McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435

    Article  CAS  Google Scholar 

  • Mercado-Blanco J, van-der-Drift KM, Olsson PE, Thomas-Oates JE, van-Loon LC, Bakker PA (2001) Analysis of the pmsCEAB gene cluster involved in biosynthesis of salicylic acid and the siderophore pseudomonine in the biocontrol strain Pseudomonas fluorescens WCS374. J Bacteriol 183:1909–1920

    Article  CAS  Google Scholar 

  • Michael RY, Nannette YY (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55:27–55

    Article  Google Scholar 

  • Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol 30:461–469

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Naegely SK (1997) Greenhouse vegetables: business is booming. Greenh Grow 15:14–18

    Google Scholar 

  • Nagarajkumar M, Bhaskaran R, Velazhahan R (2004) Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol Res 159:73–81

    Article  CAS  Google Scholar 

  • Niewiadomska A (2004) Effect of carbendazim, imazetapir and thiram on nitrogenase activity, the number of microorganisms in soil and yield of red clover (Trifolium pratense L.). Pol J Environ Stud 13:403–410

    CAS  Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125

    Article  CAS  Google Scholar 

  • Osman MS, Sivakumar D, Korsten L (2011) Effect of biocontrol agent Bacillus amyloliquefaciens and 1-methylcyclopropene on the control of postharvest diseases and maintenance of fruit quality. Crop Prot 30:173–178

    Article  CAS  Google Scholar 

  • Pavlo A, Leonid O, Iryna Z, Natalia K, Maria PA (2011) Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biol Control 56:43–49

    Article  Google Scholar 

  • Qi QG, Rose PA, Abrams GD, Taylor DC, Abrams SR, Cutler AJ (1998) (+)-Abscisic acid metabolism, 3-ketoacyl-coenzyme A synthase gene expression, and very long chain monounsaturated fatty acid biosynthesis in Brassica napus embryos. Plant Physiol 117:979–987

    Article  CAS  Google Scholar 

  • Radhakrishnan R, Shim KB, Lee BW, Hwang CD, Pae SB, Park CH, Kim SU, Lee CK, Baek IY (2013) IAA-producing Penicillium sp. NICS01 triggers plant growth and suppresses Fusarium sp.-induced oxidative stress in sesame (Sesamum indicum L.). J Microbiol Biotechnol 23:856–863

    Article  CAS  Google Scholar 

  • Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12:1633–1646

    Article  CAS  Google Scholar 

  • Reithner B, Schuhmacher R, Stoppacher N, Pucher M, Brunner K, Zeilinger S (2007) Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism and plant protection. Fungal Genet Biol 44:1123–1133

    Article  CAS  Google Scholar 

  • Rezzonico E, Flury N, Meins FJ, Beffa R (1998) Transcriptional downregulation by abscisic acid of pathogenesis-related beta-1,3-glucanase genes in tobacco cell cultures. Plant Physiol 117:585–592

    Article  CAS  Google Scholar 

  • Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol 116:387–392

    Article  CAS  Google Scholar 

  • Sharma RR, Singh D, Singh R (2009) Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biol Control 50:205–221

    Article  Google Scholar 

  • Shiau FL, Chung WC, Huang JW, Huang HC (1999) Organic amendment of commercial culture media for improving control of Rhizoctonia damping-off of cabbage. Can J Plant Pathol 21:368–374

    Article  Google Scholar 

  • Sneh B, Ichielevich-Auster M, Plaut Z (1989) Mechanisms of seedling protection by a hypovirulent isolate of Rhizoctonia solani. Can J Bot 67:2135–2141

    Article  Google Scholar 

  • Solanki MK, Kumar S, Pandey AK, Srivastava S, Singh RK, Kashyap PL, Srivastava AK, Arora DK (2012) Diversity and antagonistic potential of Bacillus spp. associated to the rhizosphere of tomato for the management of Rhizoctonia solani. Biocont Sci Technol 22:203–217

    Article  Google Scholar 

  • Stabb EV, Jacobson LM, Handelsman J (1994) Zwittermicin A producing strains of Bacillus cereus from diverse soils. Appl Environ Microbiol 60:4404–4412

    CAS  Google Scholar 

  • Thaler SJ, Bostock RM (2004) Interactions between abscisic-acid mediated responses and plant resistance to pathogens and insects. Ecology 85:48–58

    Article  Google Scholar 

  • Thimmaiah SR (1999) Standard method of biochemical analysis. Kalyani Publishers, New Delhi, pp 230–231

    Google Scholar 

  • Vicente MR, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    Article  Google Scholar 

  • Wassternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  Google Scholar 

  • Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL (2002) Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34:955–963

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by National Research Foundation of Korea (NRF), Ministry of Science, ICT and Future Planning through Basic Science Research Program (2014R1A1A1004918).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to In-Jung Lee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 509 kb)

Supplementary material 2 (DOC 31 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kang, SM., Radhakrishnan, R. & Lee, IJ. Bacillus amyloliquefaciens subsp. plantarum GR53, a potent biocontrol agent resists Rhizoctonia disease on Chinese cabbage through hormonal and antioxidants regulation. World J Microbiol Biotechnol 31, 1517–1527 (2015). https://doi.org/10.1007/s11274-015-1896-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-015-1896-0

Keywords

Navigation