Skip to main content
Log in

Chitinolytic Bacillus-Mediated Induction of Jasmonic Acid and Defense-Related Proteins in Soybean (Glycine max L. Merrill) Plant Against Rhizoctonia solani and Fusarium oxysporum

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

In the present research, bacterial-mediated elicitation of induced systemic resistance in the soybean plant was studied. The main objective was in vitro analysis of jasmonic acid and different defense-related enzymes in soybean plants primed with bacterium Bacillus sp. SJ-5 against the fungal pathogen Rhizoctonia solani and Fusarium oxysporum. In the different assays conducted, Bacillus sp. SJ-5 showed strong antifungal activity against R. solani and F. oxysporum showing 45 and 63 % growth inhibition, respectively. Strain SJ-5 was found to be positive for the cell wall-degrading enzymes chitinase, protease, and β-1,3-glucanase, and cell-free supernatant was found with significant fungal growth inhibitory activity. Different defense-related enzymes, namely lipoxygenase, phenylalanine ammonia-lyase, peroxidase, polyphenol oxidase, and β-1,3-glucanase in the different parts of Glycine max L. Merrill were reported to be highest on the 8th day after challenge inoculation and expressed significantly in the root tissue. GC–MS analysis of jasmonic acid (JA) revealed the highest JA accumulation in bacterized soybean plant root tissue challenged with R. solani and F. oxysporum, which was 91.2 and 99.84 %, respectively, with respect to control. In the SJ-5-primed root tissue, phenolic content was highest upon challenge inoculation of R. solani and F. oxysporum with 30.47 ± 0.97 and 32.4 ± 0.3 mg/g fresh weight, respectively. In summary, the present investigation revealed a role for the bacterial isolate Bacillus sp. SJ-5 in soybean plant growth promotion and enhanced protection against R. solani and F. oxysporum by elicitation of defense-related enzymes.

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
Fig. 6

Similar content being viewed by others

References

  • Abdel-Monaim MF, Mamdoh Ewis Ismail ME, Morsy KM (2012) Induction of systemic resistance in soybean plants against Fusarium wilts disease by seed treatment with benzothiadiazole and humic acid. Afr J Biotechnol 11(10):2454–2465

    CAS  Google Scholar 

  • Agrawal T, Kotasthane AS (2012) Chitinolytic assay of indigenous Trichoderma isolates collected from different geographical locations of Chhattisgarh in Central India. SpringerPlus 1(1):73

    Article  PubMed  PubMed Central  Google Scholar 

  • Akram W, Mahboob A, Javed A (2013) Bacillus thuringiensis strain 199 can induce systemic resistance in tomato against Fusarium wilt. Eur J Microbiol Immunol 3(4):275–280

    Article  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta vulgaris. Plant Physiol 24(1):1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baysal T, Demirdoven A (2007) Lipoxygenase in fruits and vegetables: a review. Enzyme Microb Technol 40(4):491–496

    Article  CAS  Google Scholar 

  • Benhamou N, Gagne S, Quere DL, Dehbi L (2000) Bacterial mediated induced resistance in cucumber: beneficial effect of the endophytic bacterium Serratia plymuthica on the protection against infection by Pythium ultimum. Phytopathol 90:45–56

    Article  CAS  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    Article  CAS  PubMed  Google Scholar 

  • Bernard E, Larkin RP, Tavantzis S, Erich MS, Alyokhin A, Sewell G, Lannan A, Gross SD (2012) Compost, rapeseed rotation, and biocontrol agents significantly impact soil microbial communities in organic and conventional potato production systems. Appl Soil Ecol 52:29–41

    Article  Google Scholar 

  • Blechert S, Brodschelm W, Hölder S, Kammerer L, Kutchan TM, Mueller MJ, Xia ZQ, Zenk MH (1995) The octadecanoic pathway: signal molecules for the regulation of secondary pathways. Proc Natl Acad Sci USA 92(10):4099–4105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205

    Article  CAS  PubMed  Google Scholar 

  • Cavalcanti FR, Oliveira JTA, Martins-Miranda AS, Vie´gas RA, Silveira JAG (2004) Superoxide dismutase, catalase and peroxidase activities do not confer protection against oxidative damage in salt stressed cowpea leaves. New Phytol 163:563–571

    Article  CAS  Google Scholar 

  • Chang WT, Chen YC, Jao CL (2007) Antifungal activity and enhancement of plant growth by Bacillus cereus grown on shellfish chitin wastes. Bioresour Techol 98:1224–1230

    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  PubMed  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clement C, Barka AE (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodd IC, Perez-Alfocea F (2012) Microbial alleviation of crop salinity stress. J Exp Bot 63:3415–3428

    Article  CAS  PubMed  Google Scholar 

  • Doornbos RF, Geraats BP, Kuramae EE, Van Loon LC, Bakker PA (2011) Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol Plant Microbe Interact 24(4):395–407

    Article  CAS  PubMed  Google Scholar 

  • Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov SZ, Lugtenberg B (2011) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fertil Soils 47(2):197–205

    Article  CAS  Google Scholar 

  • El-Abady MI, Seadh SE, Attia AN, El-Saidy Aml EA (2008) Impact of foliar fertilization and its time of application on yield and seed quality of soybean. In: The 2th field crops conference, FCRI, AV, Giza, Egypt, 14–16 Oct 2008

  • Ellis C, Karafyllidis L, Turner JG (2002) Constitutive activation of jasmonate signalling in Arabidopsis mutant correlates with enhanced resistance to Eryshiphe cichoracearum, Pseudomonas syringae and Myzus persicae. Mol Plant Microbe Interact 15:1025–1030

    Article  CAS  PubMed  Google Scholar 

  • Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol 109:813–820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-Gutiérrez L, Zeriouh H, Romero D, Cubero J, Vicente A, Pérez-García A (2013) The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate-and salicylic acid-dependent defence responses. Microb Biotechnol 6(3):264–274

    Article  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis: 2001 status. Curr Opin Plant Biol 4:301–308

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotech Adv 28(3):367–374

    Article  CAS  Google Scholar 

  • Glick BR (2015) Stress control and ACC deaminase. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Springer International Publishing, Switzerland, pp 257–264

    Google Scholar 

  • Govindappa M, Rai VR, Lokesh S (2014) Induction of resistance against Cercospora leaf spot in safflower by seed treatment with plant growth-promoting rhizobacteria. Arch Phytopathol Plant Prot 47(20):2479–2492

    Article  CAS  Google Scholar 

  • Gu XC, Chen JF, Xiao Y, Di P, Xuan HJ, Zhou X, Zhang L, Chen WS (2012) Overexpression of allene oxide cyclase promoted tanshinone/phenolic acid production in Salvia miltiorrhiza. Plant Cell Rep 31(12):2247–2259

    Article  CAS  PubMed  Google Scholar 

  • Gul A, Ozaktan H, Kidoglu F, Tuzel Y (2013) Rhizobacteria promoted yield of cucumber plants grown in perlite under Fusarium wilt stress. Sci Hortic 153:22–25

    Article  Google Scholar 

  • Heidari M, Golpayegani A (2012) Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J Saudi Soci Agric Sci 11(1):57–61

    Google Scholar 

  • Hiscox JT, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57(12):1332–1334

    Article  CAS  Google Scholar 

  • Jain S, Vaishnav A, Kasotia A, Kumari S, Gaur RK, Choudhary DK (2014) Rhizobacterium-mediated growth promotion and expression of stress enzymes in Glycine max L. Merrill against Fusarium wilt upon challenge inoculation. World J Microbiol Biotechnol 30(2):399–406

    Article  CAS  PubMed  Google Scholar 

  • Jaiti F, Verdeil JL, El Hadrami I (2009) Effect of jasmonic acid on the induction of polyphenoloxidase and peroxidase activities in relation to date palm resistance against Fusarium oxysporum f. sp. albedinis. Physiol Mol Plant Pathol 74:84–90

    Article  CAS  Google Scholar 

  • Jayaraj J, Muthukrishnan S, Liang GH, Velazhahan R (2004) Jasmonic acid and salicylic acid induce accumulation of β-1, 3-glucanase and thaumatin-like proteins in wheat and enhance resistance against Stagonospora nodorum. Biol Planta 48(3):425–430

    Article  CAS  Google Scholar 

  • Jeong MJ, Choi BS, Bae DW, Shin SC, Park SU, Lim HS, Kim J, Kim JB, Cho BK, Bae H (2012) Differential expression of kenaf phenylalanine ammo nia-lyase (PAL) ortholog during developmental stages and in response to abiotic stresses. Plant Omics 5(4):392–399

    CAS  Google Scholar 

  • Jiang K, Pi Y, Hou R, Jiang L, Sun X, Tang K (2009) Promotion of nicotine biosynthesis in transgenic tobacco by overexpressing allene oxide cyclase from Hyoscyamus niger. Planta 229(5):1057–1063

    Article  CAS  PubMed  Google Scholar 

  • Kavitha K, Mathiyazhagan S, Senthilvel V, Nakkeeran S, Chandrasekar G (2005) Development of bioformulations of antagonistic bacteria for the management of damping off of chilli (Capsicum annuum L.). Arch Phytopathol Plant Prot 38:19–30

    Article  Google Scholar 

  • Kramell R, Miersch O, Atzorn R, Parthier B, Wasternack C (2000) Octadecanoid-derived alteration of gene expression and the “oxylipin signature” in stressed barley leaves. Implications for different signaling pathways. Plant Physiol 123(1):177–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar P, Dubey RC, Maheshwari DK (2012) Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res 167:493–499

    Article  CAS  PubMed  Google Scholar 

  • Lee BK, Park MR, Srinivas B, Chun JC, Kwon IS, Chung IM, Yoo NH, Choi KG, Yun SJ (2003) Induction of phenylalanine ammonia-lyase gene expression by paraquat and stress-related hormones in Rehmannia glutinosa. Mol Cells 16(1):34–39

    CAS  PubMed  Google Scholar 

  • Liang X, Dron M, Schmid J, Dixon R, Lamb C (1989) Developmental and environmental regulation of a phenylalanine ammonia-lyase-b-glucuronidase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci USA 86:9284–9288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W, Mazarei M, Rudis MR, Fethe MH, Peng Y, Millwood RJ, Schoene G, Burris JN, Stewart CN (2013) Bacterial pathogen phytosensing in transgenic tobacco and Arabidopsis plants. Plant Biotechnol J 11(1):43–52

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lu ZX, Gaudet D, Puchalski B, Despins T, Frick M, Laroche A (2006) Inducers of resistance reduce common bunt infection in wheat seedlings while differentially regulating defence-gene expression. Physiol Mol Plant Pathol 67:138–148

    Article  Google Scholar 

  • Ludueña LM, Taurian T, Tonelli ML, Angelini JG, Anzuay MS, Valetti L, Muñoz V, Fabra AI (2012) Biocontrol bacterial communities associated with diseased peanut (Arachis hypogaea L.) plants. Eur J Soil Biol 53:48–55

    Article  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63:541–556

    Article  CAS  Google Scholar 

  • Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29(2):248–258

    Article  CAS  PubMed  Google Scholar 

  • Mayer AM, Harel E (1979) Polyphenol oxidases in plants. Phytochem 18:193–215

    Article  CAS  Google Scholar 

  • McDonald S, Prenzler PD, Antolovich M, Robards K (2001) Phenolic content and antioxidant activity of olive extracts. Food Chem 73(1):73–84

    Article  CAS  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Mori T, Sakurai M, Sakuta M (2001) Effects of conditioned medium on activities of PAL, CHS, DAHP synthase (DS-Co and DS-Mn) and anthocyanin production in suspension cultures of Fragaria ananassa. Plant Sci 160:355–360

    Article  CAS  PubMed  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M (2010) Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci Soc Am J 74(2):533–542

    Article  Google Scholar 

  • Pan SQ, Ye XS, Kuć J (1989) Direct detection of beta-1,3-glucanase isozymes on polyacrylamide electrophoresis and isoelectrofocusing gels. Anal Biochem 182(1):136–140

    Article  CAS  PubMed  Google Scholar 

  • Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265

    Article  CAS  PubMed  Google Scholar 

  • Penninckx IAMA, Eggermont K, Terras FRG, Thomma BPHJ, De Samblanx GW, Buchala A, Métraux J-P, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, Ton J, Van Loon LC (2001) Cross-talk between plant defence signalling pathways: boost or burden? AgBiotechNet 3:1–8

    Google Scholar 

  • Pineda A, Soler R, Weldegergis BT, Shimwela MM, Van Loon JJ, Dicke M (2013) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via Jasmonic acid signaling. Plant Cell Environ 36:393–404

    Article  CAS  PubMed  Google Scholar 

  • Ramamoorthy V, Raguchander T, Samiyappan R (2002) Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant Soil 239:55–68

    Article  CAS  Google Scholar 

  • Reyes-Ramirez A, Escudero-Abarca BI, Aguilar-Uscanga G, Hayward-Jones PM, Barboza-Corona JE (2004) Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J Food Sci 69:131–134

    Article  Google Scholar 

  • Rosahl S (1996) Lipoxygenases in plants: their role in development and stress response. Z Naturforsch C 51:123–138

    CAS  PubMed  Google Scholar 

  • Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29

    Article  CAS  PubMed  Google Scholar 

  • Saravitz DM, Siedow JN (1996) The differential expression of wound-inducible lipoxygenase genes in soybean leaves. Plant Physiol 110:287–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schweizer P, Buchala A, Silverman P, Seskar M, Raskin I, Metraux JP (1997) Jasmonate-inducible genes are activated in rice by pathogen attack without a concomitant increase in endogenous jasmonic acid levels. Plant Physiol 114(1):79–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senthilraja G, Anand T, Kennedy JS, Raguchander T, Samiyappan R (2013) Plant growth promoting rhizobacteria (PGPR) and entomopathogenic fungus bioformulation enhance the expression of defense enzymes and pathogenesis-related proteins in groundnut plants against leaf miner insect and collar rot pathogen. Physiol Mol Plant Pathol 82:10–19

    Article  CAS  Google Scholar 

  • Seo DJ, Nguyen DMC, Song YS, Jung WJ (2012) Induction of defense response against Rhizoctonia solani in Cucumber plants by endophytic bacterium Bacillus thuringiensis GS1. J Microbiol Biotechnol 22(3):407–415

    Article  CAS  PubMed  Google Scholar 

  • Shah J (2005) Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annu Rev Phytopathol 43:229–260

    Article  CAS  PubMed  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. Biocontrol Sci Technol 22:203–217

    Article  Google Scholar 

  • Sundaramoorthy S, Raguchander T, Ragupathi N, Samiyappan R (2012) Combinatorial effect of endophytic and plant growth promoting rhizobacteria against wilt disease of Capsicum annum L. caused by Fusarium solani. Biol Control 60(1):59–67

    Google Scholar 

  • Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5(1):51–58

    Article  CAS  Google Scholar 

  • Thomma BPHJ, Penninckx IAMA, Cammue BPA, Broekaert WF (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68

    Article  CAS  PubMed  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  PubMed  Google Scholar 

  • Vick BA, Zimmerman DC (1984) Biosynthesis of jasmonic acid by several plant species. Plant Physiol 2:458–461

    Article  Google Scholar 

  • Vijayan P, Shockey J, Lévesque A, Cook RJ, Browse J (1998) A role for jasmonates in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA 95:7209–7214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vincent JM (1947) Distortion of fungal hyphae in the presence ofcertain inhibitors. Nature 159:850

    Article  CAS  PubMed  Google Scholar 

  • Wahyudi AT, Astuti RP, Widyawati A, Meryandini A, Nawangsih AA (2011) Characterization of Bacillus sp. strains isolated from rhizosphere of soybean plants for their use as potential plant growth for promoting Rhizobacteria. J Microbiol Antimicrob 3(2):34–40

    Google Scholar 

  • Walia A, Mehta P, Chauhan A, Shirkot CK (2013) Antagonistic Activity of plant growth promoting rhizobacteria isolated from tomato rhizosphere against soil borne fungal plant pathogens. Int J Agric Environ Biotechnol 6(4):571–580

    Article  Google Scholar 

  • Wang SL, Hsiao WJ, Chang WT (2002) Purification and characterization of an antimicrobial chitinase extracellularly produced by Monascus purpureus CCRC31499 in a shrimp and crab shell powder medium. J Agric Food Chem 50:2249–2255

    Article  CAS  PubMed  Google Scholar 

  • Weller DM (1988) Biological control of soil borne plant pathogens in rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407

    Article  Google Scholar 

  • Yang DH, Hettenhausen C, Baldwin IT, Wu JQ (2011) BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata’s responses to herbivory. J Exp Bot 62:641–652

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The research was supported by DBT Grant No. BT/PR1231/AGR/21/340/2011 to DKC. Some of the research has been supported by SERB-DST Grant No. SR/FT/LS-129/2012 to DKC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Devendra Kumar Choudhary.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jain, S., Vaishnav, A., Kumari, S. et al. Chitinolytic Bacillus-Mediated Induction of Jasmonic Acid and Defense-Related Proteins in Soybean (Glycine max L. Merrill) Plant Against Rhizoctonia solani and Fusarium oxysporum . J Plant Growth Regul 36, 200–214 (2017). https://doi.org/10.1007/s00344-016-9630-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-016-9630-1

Keywords

Navigation