Log in

Characterization and evaluation of extracellular hydrolytic proteins from rhizobacterial antagonists isolated from Fusarium oxysporum f. sp. ciceris infected chickpea fields

  • Research Article
  • Published:
Indian Phytopathology Aims and scope Submit manuscript

Abstract

In the present study, twenty-six rhizobacterial antagonists of Fusarium oxysporum f. sp. ciceris (Foc), isolated from Foc infected chickpea fields were evaluated for their protein secretion. Exoprotein liberation by rhizobacterial antagonists lied in the range between 28.2 and 795 μg/ml, where maximum exoprotein was recorded by isolate Ps47, followed by Ps45 (795.0 µg/ml) and Ps44 (578.2 μg/ml). Further observation of hydrolytic proteins, revealed most of the bacterial antagonists to exhibit proteolytic, amylolytic, chitinolytic as well as cellulose degrading potential on minimal agar plates, supplemented with respective substrates. About 73 and 80% of the antagonists were found positive for chitinolytic and cellulolytic activity respectively, where isolate Ba18 scored maximum hydrolytic index for chitin and Ba10 exhibited highest cellulose hydrolytic index of 2.1. Assay for proteases, denoted 84.6% of isolates to produce lysis zones, when gelatin was used as protein source, where 80% of isolates showed hydrolytic activity for casein supplemented minimal salt (MS) agar. SDS-PAGE analysis for the presence of hydrolytic enzymes in the extracellular crude protein revealed Pseudomonas isolate Ps45 and Bacillus Ba1a to exhibit a range of protein bands between 5 and 150 kDa, belonging to several group of proteases, amylases, chitinases and cellulases. Scanning Electron Microscopic examinations of the interaction zones between fungal pathogen (Foc) and isolate Ps45, revealed hyphal distortion due to lysis effect with scanty mycelial growth compared to control, that was maintained without any bacterial treatment. Screening and characterization of bacterial strains with the ability to produce a range of lytic enzymes will greatly enhance our understanding for their exploitation in the management of soil borne fungal pathogens.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdel-Monaim MF, Mahmoud E, Ibrahim M, Fatma AM, Zeinab NH, Soliman S, Sobeiha A, Fatma M, Waked DA, Eleawa M, Salama A (2016) Efficacy of secondary metabolites and extracellular lytic enzymes of plant growth promoting rhizobacteria (PGPR) in controlling fusarium wilt of chickpea. Egypt J Agric Res 94(3):573–589

    Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and application s of plant growth promoting rhizobacteri a: current perspective. J King Saud Univ Sci 26:1–20

    Article  Google Scholar 

  • Ajit NS, Verma R, Shanmugam V (2006) Extracellular chitinases of fluorescent pseudomonads antifungal to Fusarium oxysporum f. sp. dianthi causing carnation wilt. Curr Microbiol 52(4):310–316

    Article  CAS  PubMed  Google Scholar 

  • Akbalık G (2003) Screening for industrially important extracellular enzymes from alkalophilic Bacillus genus, Master’s thesis, İzmir Institute of Technology.

  • Annamalai N, Rajeswari MV, Balasubramanian T (2014) Extraction, purification and application of thermostable and halostable alkaline protease from Bacillus alveayuensis CAS 5 using marine waste. Food Bioprod Process 92:335–342

    Article  CAS  Google Scholar 

  • Ardura A, Ana LR, Vazquez EG (2013) Genetic detection of Pseudomonas spp. in commercial amazonian fish. Int J Environ Res Public Health 10:3954–3966

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Avinash TS, Rai VR (2016) Plant growth promoting rhizobacteria: a boon to agriculture. Int J Agric Food Sci 6(2):28–36

    Google Scholar 

  • Aziz LM, Hamza SJ, Rahman AA (2012) Isolation and characterization of phenazine produced from mutant Pseudomonas aeruginosa. Al Anbar J Vet Sci 5(1):42–52

    Google Scholar 

  • Bach ED, Santos SGD, de Carvalho FG, Lisboa BB, Passaglia LMP (2016) Evaluation of biological control and rhizosphere competence of plant growth promoting bacteria. Appl Soil Ecol 99:141–149

    Article  Google Scholar 

  • Basha S, Ulaganathan K (2002) Antagonism of Bacillus species (strain BC121) towards Curvularia lunata. Curr Sci 25:1457–1463

    Google Scholar 

  • Brzezinska MS, Jankiewicz U, Burkowska A, Walczak M (2014) Chitinolytic microorganisms and their possible application in environmental protection. Curr Microbiol 68(1):71–81

    Article  CAS  Google Scholar 

  • Chaiharn M, Chunhaleuchanon S, Kozo A, Lumyong S (2008) Screening of rhizobacteria for their plant growth promoting activities. Curr Appl Sci Technol 8(1):18–23

    Google Scholar 

  • Chang WT, Wag CM (2010) An antifungal chitinase produced by Bacillus subtilis using chitin waste as a crabon source. World J Microbiol Biotechnol 26:945–950

    Article  CAS  Google Scholar 

  • Chao-Lin L, Chia-Rui S, Fong-Fu H, Jeen-Kuan C, Pei-Tzu W, Shang- Hsin G, Wen-Chien L, Feng-Wei Y, Zachary BM, John T, Grosx ML (2009) Isolation and identification of two novel SDS-resistant secreted chitinases from Aeromonas schubertii. Biotechnol Prog 25(1):124–131

    Article  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 71:4951–4959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunne C, Moe-Loccoz Y, Bruijn FJ, O’Gara F (2000) Overproduction of an inducible extracellular serine protease improves biological control of Pythium ultimum by Stenotrophomonas maltophilia strain W81. Microbiology 146:2069–2078

    Article  CAS  PubMed  Google Scholar 

  • Fernando WGD, Nakkeeran S, Zhang Y (2006) Biosynthesis of antibiotics by PGPR and its relation in biocontrol of plant diseases. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Netherlands, pp 67–109

    Chapter  Google Scholar 

  • Fira D, Dimkić I, Berić T, Lozo J, Stanković S (2018) Biological control of plant pathogens by Bacillus species. J Biotechnol 285:44–55

    Article  CAS  PubMed  Google Scholar 

  • Gajera HP, Savaliya DD, Hirapara DG, Patel SV, Golakiya BA (2016) Biocontrol mechanism of bacillus for fusarium wilt management in cumin (Cuminum cyminum L.). Current trends in plant disease diagnostics and management practices. Springer, Cham, pp 29–47

    Chapter  Google Scholar 

  • Gomez-Ramırez M, Rojas-Avelizapa LI, Rojas-Avelizapa NG, Cruz-Camarillo RC (2004) Colloidal chitin stained with Remazol Brilliant Blue R, a useful substrate to select chitinolytic microorganisms and to evaluate chitinases. J Microbiol Methods 56:213–219

    Article  PubMed  CAS  Google Scholar 

  • Gopalakrishnan S, Vadlamudi S, Samineni S, Kumar CVS (2016) Plant growth-promotion and biofortification of chickpea and pigeonpea through inoculation of biocontrol potential bacteria, isolated from organic soils. Springer plus 5:1882–1893

    Article  PubMed  PubMed Central  Google Scholar 

  • Granjo CA, Dos RTA, Gambale W, Corrêa B (2007) Morphogenesis and growth kinetics of Fusarium verticillioides. Mycopathologia 164(3):119–126

    Article  PubMed  Google Scholar 

  • Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7(2):96–102

    CAS  Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion. A review. Ann Microbiol 60(4):5795–5798

    Article  Google Scholar 

  • Huang LQ, Niu YC, Su L, Deng H, Lyu H (2020) The potential of endophytic fungi isolated from cucurbit plants for biocontrol of soilborne fungal diseases of cucumber. Microbiol Res 231:126369

    Article  CAS  PubMed  Google Scholar 

  • Jadhav HP, Shaikh SS, Sayyed RZ (2017) Role of hydrolytic enzymes of rhizoflora in biocontrol of fungal phytopathogens: an overview. Rhizotrophs: plant growth promotion to bioremediation. Springer, Singapore, pp 183–203

    Chapter  Google Scholar 

  • Jensen DF, Karlsson M, Sarrocco S, Vannacci G (2016) Biological control using microorganisms as an alternative to disease resistance. Plant Pathogen Resistance Biotechnol 341–363

  • Joshi M, Shrivastava R, Sharma AK, Prakash A (2012) Screening of resistant verities and antagonistic Fusarium oxysporum for biocontrol of Fusarium Wilt of Chilli. Plant Pathol Microbiol 3(134):2

    Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360

    Article  CAS  PubMed  Google Scholar 

  • Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol Biochem 35:323–331

    Article  CAS  Google Scholar 

  • Kim YC, Glick B, Bashan Y, Ryu CM (2013) Enhancement of plant drought tolerance by microbes. In: Aroca R (ed) Plant responses to drought stress. Springer, Berlin, pp 45–51

    Google Scholar 

  • Kohring S, Wiegel J, Mayer F (1990) Subunit composition and glycosidic activities of the cellulase complex from Clostridium thermocellum JW20. Appl Environ Microbiol 56(12):3798–3804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar PA, Johri BN (2011) Bacillus as PGPR in crop ecosystem. In: Maheshwari DK (ed) Bacteria in agrobiology: crop ecosystems. Springer, Berlin, pp 37–59

    Chapter  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(8):493–499

    Article  CAS  PubMed  Google Scholar 

  • Kumari S, Khanna V (2014) Effect of antagonistic rhizobacteria coinoculated with Mesorhizobium ciceris on control of fusarium wilt in chickpea (Cicer arietinum L.). Afric J Micro Res 8(12):1255–1265

    Article  Google Scholar 

  • Kumari S, Khanna V (2018) Biological management of vascular wilt of chickpea (Cicer arietinum L.) incited by Fusarium oxysporum f. sp. ciceris by antagonistic rhizobacteria co-inoculated with native mesorhizobium. Int J Curr Microbiol App Sci 7(1):920–941

    Article  CAS  Google Scholar 

  • Kumari S, Khanna V (2019) Biocidal mechanisms in biological control of fusarium wilt in chickpea (Cicer arietinum L.) by antagonistic rhizobacteria: a current perspective in soil borne fungal pest management. Int J Curr Microbiol App Sci 8(10):1494–1510

    Article  CAS  Google Scholar 

  • Kumari S, Khanna V (2020) Induction of systemic resistance in chickpea (Cicer arietinum L.) against Fusarium oxysporum f. sp. ciceris by antagonistic rhizobacteria in assistance with native mesorhizobium. Curr Microbiol 77(1):85–98

    Article  CAS  PubMed  Google Scholar 

  • Kumari P, Khanna V, Sharma P, Kumari S (2016) Allelopathic effects of native Bacillus sp. against Fusarium oxysporum causing chickpea wilt. Allelopath J 38:77–90

    Google Scholar 

  • Kumudini BS, Jayamohan NS, Patil SV (2017) Integrated mechanisms of plant disease containment by rhizospheric bacteria: Unraveling the signal cross talk between plant and fluorescent Pseudomonas. In: Agriculturally important microbes for sustainable agriculture. Springer, Singapore, pp. 263–291

  • Leon M, Yaryura PM, Montecchia MS, Hernandez AI, Correa OS, Pucheu NL, Kerber NL, Garcia AF (2009) Antifungal activity of selected indigenous Pseudomonas and Bacillus from the soybean rhizosphere. Int J Microbiol 5:1–9

    Article  Google Scholar 

  • Lowry OH, Rosbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with Folin Phenol reagent. J Biol Chem 193:265–370

    Article  CAS  PubMed  Google Scholar 

  • Maharana AK, Ray P (2013) Isolation and screening of cold active extracellular enzymes producing psychrotrophic bacteria from soil of Jammu City. Biosci Biotechnol Res Asia 10(1):267–273

    Article  Google Scholar 

  • Maksimov I, Abizgildina RR, Pusenkova LI (2011) Plant growth promoting rhizobacteria as alternative to chemical crop protectors from pathogens. Appl Biochem Microbiol 47:333–345

    Article  CAS  Google Scholar 

  • Mala M, Srividya S (2010) Partial purification and properties of a laundry detergent compatible alkaline protease from a newly isolated Bacillus species Y. Indian J Microbiol 50:309–317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manjula K, Poldile AR (2005) Production of fungal cell wall degrading enzymes by biocontrol strain of Bacillus subtilis A F 1. Indian J Exp Biol 43:892–896

    CAS  PubMed  Google Scholar 

  • Nadeem SM, Naveed M, Zahir ZA, Asghar HN (2013) Plant–microbe interactions. Plant microbe symbiosis: fundamentals and advances. Springer, India, pp 51–103

    Chapter  Google Scholar 

  • Namasivayam E, Ravindar JD, Mariappan K, Akhil J, Mukesh K, Jayara R (2011) Production of extracellular pectinase by Bacillus cereus isolated from market solid waste. J Bioanal Biomed 3(3):70–75

    Article  Google Scholar 

  • Neeraja C, Anil K, Purushotham P, Suma K, Sarma P, Moerschbacher BM, Podile AR (2010) Biotechnological approaches to develop bacterial chitinases as a bioshield against fungal diseases of plants. Crit Rev Biotechnol 30:231–241

    Article  CAS  PubMed  Google Scholar 

  • Nion YA, Toyota K (2015) Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ. p ME14144

  • Pande S, Desai S, Sharma M (2010) Impacts of climate change on rainfed crop diseases: Current Status and Future Research Needs. Nat Symp Clim Change Rainfed Agric Hyderabad 18(20):55–59

    Google Scholar 

  • Pushpavathi Y, Dash SN, Madhavi N, Deepika D (2016) Biological control of Fusarium wilt disease in banana with emphasis on Trichoderma spp. and Pseudomonas spp. Plant Arch 16(1):51–59

    Google Scholar 

  • Radjacommare R, Venkatesan S, Samiyappan R (2010) Biological control of phytopathogenic fungi of vanilla through lytic action of Trichoderma species and Pseudomonas fluorescens. Arch Phytopathol Pflanzenschutz 43(1):1–17

    Article  CAS  Google Scholar 

  • Rajput RS, Singh P, Singh J, Ray S, Vaishnav A, Singh HB (2019) Seed biopriming through beneficial rhizobacteria for mitigating soil-borne and seed-borne diseases. In: Plant growth promoting rhizobacteria for sustainable stress management. Springer, Singapore. pp. 201–215

  • Ramesh R, Mathew T, Singh N (2009) Role of chitinolytic enzymes and volatile compounds produced by endophytic bacteria in the inhibition of mango (Mangifera indica L.) root rot pathogens. J Biol Control 23(4):433–441

    Google Scholar 

  • Raza W, Ling N, Zhang R, Huang Q, Xu Y, Shen Q (2017) Success evaluation of the biological control of Fusarium wilts of cucumber, banana, and tomato since 2000 and future research strategies. Crit Rev Biotechnol 37(2):202–212

    Article  PubMed  Google Scholar 

  • Rezzonico F, Zala M, Keel C, Duffy B, Moénne-Loccoz Y, Défago G (2007) Is the ability of biocontrol fluorescent pseudomonads to produce the antifungal metabolite 2, 4-diacetylphloroglucinol really synonymous with higher plant protection. New Phytol 173:861–872

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Sanchez A, Cruz-Camarillo R, Salcedo-Hernandez R, Barboza-Corona JE (2005) Chitinases from Serratia marcescens Nima. Biotechnol Lett 27:649–653

    Article  CAS  PubMed  Google Scholar 

  • Sabaratnam S, Traquair JA (2015) Mechanism of antagonism by Streptomyces griseocarneus (strain Di944) against fungal pathogens of greenhouse-grown tomato transplants. Can J Plant Pathol 37(2):197–211

    Article  CAS  Google Scholar 

  • Sadfi N, Cherif M, Hajlaoui MR, Boudabbous A, Belanger R (2002) Isolation and partial purification of antifungal metabolites produced by Bacillus cereus. Ann Microbiol 52(3):323–338

    CAS  Google Scholar 

  • Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169(1):18–29

    Article  CAS  PubMed  Google Scholar 

  • Sarian FD, van der Kaaij RM, Kralj S, Wijbenga DJ, Binnema DJ, Vander MMJ, Dijkhuizen L (2012) Enzymatic degradation of granular potato starch by Microbacterium aurum strain B8A. Appl Microbiol Biotechnol 93(2):645–654

    Article  CAS  PubMed  Google Scholar 

  • Sasirekha B, Bedashree T, Champa KL (2012) Optimization and partial purification of extracellular phytase from Pseudomonas aeruginosa p6. Eur J Exp Biol 2(1):95–104

    CAS  Google Scholar 

  • Schallmey M, Singh A, Ward OP (2004) Development in the use of Bacillus sp. for industrial production. Cna J Microbiol 50:1–9

    Article  CAS  Google Scholar 

  • Sekhon A, Dahiya N, Tewari RP, Hoondal GS (2006) Production of extracellular lipase by Bacillus megaterium AKG-1 in submerged fermentation. Indian J Biotechnol 5:179–183

    CAS  Google Scholar 

  • Shahbazi M, Reza H, Heidari K (2012) A novel low molecular weight extracellular protease from a moderately halophilic bacterium Salinivibrio sp. strain MS-7: production and biochemical properties. Mol Biol Res Comm 1(2):45–56

    Google Scholar 

  • Shalini SR (2007) Screening for antifungal activity of pseudomonas fluorescens against phytopathogenic fungi. Internet J Microbiol 5(2):1–6

    Google Scholar 

  • Silva AKS, Silva TRN, Nicoli JR, Vasquez-Pinto LMC, Martins FS (2018) In vitro evaluation of antagonism, modulation of cytokines and extracellular matrix proteins by Bifidobacterium strains. Lett Appl Microbiol 67(5):497–505

    Article  CAS  PubMed  Google Scholar 

  • Sindhu SS, Dadarwal KR (2001) Chitinolytic and cellulolytic Pseudomonas sp. antagonistic to fungal pathogens enhances nodulation by Mesorhizobium sp. cicer in chickpea. Microbiol Res 156(4):353–358

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Jain A, Sarma BK, Upadhyay RS, Singh HB (2014) Rhizosphere competent microbial consortium mediates rapid changesin phenolic profiles in chickpea during Sclerotium rolfsii infection. Microbiol Res 169:353–360

    Article  CAS  PubMed  Google Scholar 

  • Sku** JJ, Potgieter HJ, Alexunder M (1965) Dissolution of fungal cell wall by Streptomyces Chitinase and β(1–3) glucanase. Arch Biochem Biophy 111:358–364

    Article  Google Scholar 

  • Smolińska U, Kowalska B (2018) Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum––a review. J Pl Pathol 100(1):1–12

    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. Biocontrol Sci Tech 22(2):203–217

    Article  Google Scholar 

  • Spilker T, Coenye T, Vandamme P, LiPuma JJ (2004) PCR-based assay for differentiation of Pseudomonas aeruginosa from other Pseudomonas species recovered from cystic fibrosis patients. J Clin Microbiol 42:2074–2079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutrisno A, Ueda M, Abe Y, Nakazawa M, Miyatake KA (2004) Chitinase with high activity toward partially N-acetylated chitosan from a new, moderately thermophilic, chitin-degrading bacterium, Ralstonia sp. A-471. Appl Microbiol Biotechnol 63:398–406

    Article  CAS  PubMed  Google Scholar 

  • Trotel-Aziz P, Couder M, Biagianti S, Aziz A (2008) Characterisation of new bacterial biocontrol agents Acinetobacter, Bacillus, Pantoea and Pseudomonas sp. mediating grapevine resistance against Botrytis cinerea. Environ Exp Bot 64:21–32

    Article  Google Scholar 

  • Ueda M, Kotani Y, Sutrisno A, Nakazawa M, Miyatake K (2005) Purification and characterization of chitinase b from moderately thermophilic bacterium Ralstonia sp. A-471. Biosci Biotechnol Biochem 69(4):842–844

    Article  CAS  PubMed  Google Scholar 

  • Upadyay SK, Maurya SK, Singh DP (2012) Salinity tolerance in free living plant growth promoting Rhizobacteria. Ind J Sci Res 3:73–78

    Google Scholar 

  • Wang N, Liu M, Guo L, Yang X, Qiu D (2016) A novel protein elicitor (PeBA1) from Bacillus amyloliquefaciens NC6 induces systemic resistance in tobacco. Int J Biol Sci 12(6):757–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • **an L, Wang F, Luo X, Feng YL, Feng JX (2015) Purification and characterization of a highly efficient calcium-independent α-amylase from Talaromyces pinophilus. PLoS ONE 10(3):1–95

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The present investigation was conducted at Pulses section, Department of Plant Breeding and Genetics, Punjab Agricultural University. The authors are thankful to Department of Microbiology, Punjab Agricultural University, Ludhiana, Punjab, India for further support and Department of Science and Technology (DST), New Delhi, for funding as doctoral fellowship to the first as well as the corresponding author of the manuscript.

Funding

The authors are thankful to Punjab Agricultural University, Ludhiana, Punjab, India for providing facilities and Department of Science and Technology (DST), New Delhi, for funding as doctoral fellowship to the first as well as the corresponding author of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

First author: Dr. (Mrs.) SK (Corresponding Author). Specific contribution: Planning and execution of the represented research work, Writing and editing of the manuscript. Second author: Dr. (Mrs.) VK. Specific contribution: Planning of the experiments included in this study, reviewing the manuscript. Third author: Dr. AS. Specific contribution: Assistance in the experiments especially SDS-PAGE analysis included in this study.

Corresponding author

Correspondence to Suman Kumari.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. The first author Dr. Suman Kumari declares that she has no conflict of interest. The second author Dr. Veena Khanna declare that she has no conflict of interest and the third author Dr. Alla Singh also declare that he has no conflict of interest.

Ethics approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Consent to participate

All the persons that have contributed to this manuscript are presented as authors in series according to his her/ contribution. There is no other person that has contributed and is not acknowledged. All the authors agree for their place in author list as presented/submitted.

Consent for publication

The corresponding author declare that no content/data or material has been presented in the manuscript other than the corresponding author’s of only this manuscript (with reference). All the authors declare the same.

Availability of data and material

The authors declare that the data supporting the findings of this study are available within the article itself.

Code availability

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumari, S., Khanna, V. & Singh, A. Characterization and evaluation of extracellular hydrolytic proteins from rhizobacterial antagonists isolated from Fusarium oxysporum f. sp. ciceris infected chickpea fields. Indian Phytopathology 75, 165–177 (2022). https://doi.org/10.1007/s42360-021-00443-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42360-021-00443-y

Keywords

Navigation