Skip to main content
SpringerLink
Log in

Antagonist capacity of bacteria isolated from cape gooseberry cultures (Physalis peruviana L.) for biological control of Fusarium oxysporum

  • Original Article
  • Published:
Tropical Plant Pathology Aims and scope Submit manuscript

Abstract

Vascular wilt caused by Fusarium oxysporum is the most damaging disease in cape gooseberry (Physalis peruviana L.) production. In this study, we isolated and biochemically characterized endophytes and rhizospheric bacterial isolates with antagonistic activity against F. oxysporum from cape gooseberry plants. Bacterial isolates were evaluated under in vitro conditions for their antagonistic capacity against a highly virulent isolate of F. oxysporum, as well as production of lytic enzymes, biosurfactants and volatile organic compounds. Twenty-four antagonistic bacteria were selected, out of which Bacillus sp. MB015 and Pseudomonas sp. MB108 exhibited the best biocontrol activity in vitro, with inhibition levels of 80.6% and 79.9%, respectively. However, under greenhouse conditions, P. fluorescens MB103 and B. megaterium MB112 presented the best antagonistic capacity with 83.3% control of vascular wilt incidence. P. fluorescens MB103 was one of most effective in reducing the disease severity with an area under the disease of progress curve (AUDPC) of 7.5, compared with the negative control (soil infested with Fox17 without test bacteria), which presented an AUDPC of 36.8. These results suggest that P. fluorescens MB103 is a good candidate for use as a biocontrol agent against vascular wilt caused by F. oxysporum in cape gooseberry under field conditions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abdallah A, Jabnoun-Khiareddine H, Nefzi A, Mokni-Tlili S, Daami-Remadi M (2016) Endophytic Bacteria from Datura stramonium for Fusarium Wilt Suppression and Tomato Growth Promotion. Journal of Microbial & Biochemical Technology 8:030–041

    Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arun M, Asha V (2007) Preliminary studies on antihepatotoxic effect of Physalis peruviana Linn. (Solanaceae) against carbon tetrachloride induced acute liver injury in rats. Journal of Ethnopharmacology 111:110–114

    CAS  PubMed  Google Scholar 

  • Bravo K, Sepulveda-Ortega S, Lara-Guzman O, Navas-Arboleda A, Osorio E (2015) Influence of cultivar and ripening time on bioactive compounds and antioxidant properties in Cape gooseberry (Physalis peruviana L.). Journal of the Science of Food and Agriculture 95:1562–1569

    CAS  PubMed  Google Scholar 

  • Chandran S, Parmeswaran B, Pandey A (2007) Microbial chitinases: Effective biocontrol agents. In: Chincholkar S, Mukerji K (eds) Biological Control of Plant Disease. The Haworth Press, Philadelphia, pp 379–400

    Google Scholar 

  • Chen X, 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. Nature Biotechnology 25:1007–1014

    CAS  PubMed  Google Scholar 

  • Chen F, Wang M, Zheng Y, Luo J, Yang X, Wang X (2010) Quantitative changes of plant defense enzymes and phytohormone in biocontrol of cucumber Fusarium wilt by Bacillus subtilis B579. World Journal of Microbiology and Biotechnology 26:675–684

    CAS  Google Scholar 

  • Chowdhury SP, Hartmann A, Gao X, Borriss R (2015) Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review. Frontiers in Microbiology 6:780

    PubMed  PubMed Central  Google Scholar 

  • Chung WH, Chung WC, Ting PF, Ru CC, Huang HC, Huang JW (2009) Nature of resistance to methyl benzimidazole carbamate fungicides in Fusarium oxysporum f. sp. lilii and F. oxysporum f. sp. gladioli in Taiwan. Journal of Phytopathology 157:742–747

    CAS  Google Scholar 

  • Cole SE, LaRiviere FJ, Merrikh CN, Moore MJ (2009) A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Molecular Cell 34:440–450

    CAS  PubMed  PubMed Central  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka E (2005) Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects. Applied and Environmental Microbiology 71:4951–4959

    CAS  PubMed  PubMed Central  Google Scholar 

  • D’aes J, Maeyer KD, Pauwelyn E, Hofte M (2010) Biosurfactants in plant Pseudomonas interactions and their importance to biocontrol. Environmental Microbiology Reports 2:359–372

    PubMed  Google Scholar 

  • Dean R, Kan J, Pretorius Z, Hammond-Kosack K, Pietro A, Spanu P et al (2012) The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13:414–430

    PubMed  PubMed Central  Google Scholar 

  • De Boer M, van der Sluis L, van Loon L, Bakker P (1999) Combining fluorescent Pseudomonas spp. strains to enhance suppression of fusarium wilt of radish. European Journal of Plant Pathology 105:201–210

    Google Scholar 

  • Döbereiner J, Baldani V, Baldani J (1995) Como isolar e identificar bactérias diazotróficas de plantas não-leguminosas. Embrapa – CNPAB. 60 p

  • Domsh K, Gams W, Anderson T (1980) Compendium of soil fungi, volume 1, part I, Ed. Academic Press, London, p 430

    Google Scholar 

  • Duijff B, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. The New Phytologist 135:325–334

    CAS  Google Scholar 

  • Fisher G, Almanza-Merchán P, Miransa D (2014) Importancia y cultivo de la Uchuva (Physalis peruviana L.). Rev. Bras. Frutic., Jaboticabal - SP, 36: 001-015

  • Enciso-Rodríguez F, González C, Rodríguez E, López C, Landsman D, Barrero L, Mariño-Ramírez L (2013) Identification of immunity related genes to study the Physalis peruviana – Fusarium oxysporum pathosystem. PlosOne 8:1–11

    Google Scholar 

  • Gasztonyi M, Josepovits G, Molnar A, Hornok L (1987) Biochemical background of resistance to benomyl in genetically different strains of Fusarium oxysporum. Pesticide Biochemistry and Physiology 29:17–24

    CAS  Google Scholar 

  • Gómez-Lama C, Schilirò E, Valverde-Corredor A, Mercado-Blanco J (2014) The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Frontiers in Microbiology 5:427

    Google Scholar 

  • Hallmann J, Berg G (2006) Spectrum and population dynamics of bacterial root endophytes. In: Schulz B, Boyle C, Sieber TN (eds) Soil Biology. Microbial Root Endophytes, Springer, United States, pp 15–32

    Google Scholar 

  • Jha P, Gupta G, Jha P, Mehrotra R (2013) Association of rhizospheric/endophytic bacteria with plants: A potential gateway to sustainable agriculture. Greener Journal of Agricultural Sciences 3:73–84

    Google Scholar 

  • Jholapara R, Mehta R, Sawant C (2013) Optimization of cultural conditions for chitinase production from chitinolytic bacterium isolated from soil sample. Int. J. Pharm. Biol. Sci. 4(2):464–471

    CAS  Google Scholar 

  • Kejela T, Thakkar V, Patel R (2017) A novel strain of Pseudomonas inhibits Colletotrichum gloeosporioides and Fusarium oxysporum infections and promotes germination of coffee. Rhizosphere 4:9–15

    Google Scholar 

  • Kim B, Lee J, Hwang B (2000) In vivo control and in vitro antifungal activity of rhamnolipid B, a glycolipid antibiotic, against Phytophthora capsici and Colletotrichum orbiculare. Pest Management Science 56:1029–1035

    CAS  Google Scholar 

  • Kim P, Ryu J, Kim Y, ChI Y (2010) Production of biosurfactant lipopeptides Iturin A, Fengycin, and Surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. Journal of Microbiology and Biotechnology 20:138–145

    CAS  PubMed  Google Scholar 

  • Kloepper J, Ryu C (2006) Bacterial endophytes as elicitors of induced systemic resistance. In: Schulz B, Boyle C, Sieber TN (eds) Soil Biology. Microbial Root Endophytes Springer, United States, pp 33–52

    Google Scholar 

  • Leslie J, Summerell B (2006) The Fusarium laboratory manual, 1st edition, Ed. Blackwell Publishing Professional, Manhattan, 387 p

    Google Scholar 

  • Madigan M, Martinko J, Parker J (2006) Brock Biology of Microorganisms, 11th edn. Prentice Hall Iberia, Madrid

    Google Scholar 

  • Mahaffee W, Kloepper J (1997) Temporal changes in the bacterial communities of soil, rhizosphere, and endorhiza associated with field-grown cucumber (Cucumis sativus L.). Microbial Ecology 34:210–223

    CAS  PubMed  Google Scholar 

  • Maheshwari D, Dubey R, Agarwal M, Dheeman S, Aeron A, Bajpai V (2015) Carrier based formulations of biocoenotic consortia of disease suppressive Pseudomonas aeruginosa KRP1 and Bacillus licheniformis KRB1. Ecological Engineering 81:272–277

    Google Scholar 

  • Mazzola M, Zhao X, Cohen MF, Raaijmakers JM (2007) Cyclic lipopeptide surfactant production by Pseudomonas fluorescens SS101 is not required for suppression of complex Pythium spp. populations. Phytopathology 97:1348–1355

    CAS  PubMed  Google Scholar 

  • Mendiburu F (2012) Package Agricolae-Statistical Procedures for Agricultural Research Version 1.1-2. http://cran.r-project.org/web/packages/agricolae/index.html

  • Montealegre J, Reyes R, Peréz L, Herrera R, Silva P, Besoain X (2003) Selection of bioantagonistic bacteria to be used in biological control of Rhizoctonia solani in tomato. Electronic Journal of Biotechnology 6:115–127

    Google Scholar 

  • Naing K, Lee Y, Kim M, Nguyen X, Kim Y, Kim Y et al (2015) Biocontrol of Fusarium wilt disease in tomato by Paenibacillus ehimensis KWN38. World Journal of Microbiology and Biotechnology 31:165–174

    CAS  PubMed  Google Scholar 

  • Narayanasamy P (2013a) Detection and identification of bacterial biological control agents. In: Narayanasamy P (ed) Biological Management of Diseases of Crops. Springer, Dordrecht, pp 201–294

    Google Scholar 

  • Narayanasamy P (2013b) Mechanisms of action of bacterial biological control agents. In: Narayanasamy P (ed) Biological Management of Diseases of Crops. Springer, Dordrecht, pp 295–429

    Google Scholar 

  • Ommati F, Zaker M, Mohammadi A (2013) Biological control of Fusarium wilt of potato (Fusarium oxysporum f. sp. tuberosi) by Trichoderma isolates under field condition and their effect on yield. Journal of Crop Protection 2:435–442

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Osorio-Guarín J, Encizo-Rodríguez F, González C, Fernández-Pozo N, Mueller L, Barrero L (2016) Association analysis for disease resistance to Fusarium oxysporum in cape gooseberry (Physalis peruviana L). BMC Genomics 17:248

    PubMed  PubMed Central  Google Scholar 

  • Özyilmaz Ü, Benlioglu K (2013) Enhanced biological control of Phytophthora blight of pepper by biosurfactant-producing Pseudomonas. Plant Pathology Journal 29:418–426

    PubMed  Google Scholar 

  • R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/

  • Raaijmakers J, Paulitz T, Steinberg C, Alabouvette C (2009) The Rhizosphere: A Playground and battlefield for soilborne pathogens and benefical microorganisms. Plant and Soil 321:341–361

    CAS  Google Scholar 

  • Ramadan M (2011) Bioactive phytochemicals, nutritional value, and functional properties of cape gooseberry (Physalis peruviana): An overview. Food Research International 44:1830–1836

    CAS  Google Scholar 

  • Ramyabharathi S, Meena B, Raguchander T (2012) Induction of chitinase and β-1, 3-glucanase PR proteins in tomato through liquid formulated Bacillus subtilis EPCO 16 against Fusarium wilt. Journal of Today’s Biological Sciences: Research & Review 1:50–60

    Google Scholar 

  • Ryan R, Germaine K, Franks A, Ryan D, Dowling D (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiology Letters 278:1–9

    CAS  PubMed  Google Scholar 

  • Salazar L, Patiño L, Bustamante E (2006) Sustratos foliares para el incremento de bacterias quitinolíticas y glucanolíticas en la filósfera de banano. Revista Facultad Nacional de Agronomía 59:3449–3465

    Google Scholar 

  • Salazar M, Jones J, Chaves B, Cooman A (2008) A model for the potential production and dry matter distribution of Cape gooseberry (Physalis peruviana L.). Scientia Horticulturae 115:142–148

    Google Scholar 

  • Sambrook J, Maccallum P, Russel D (2001) Molecular cloning: A laboratory manual, 3nd edn. Cold Springs Harbour Press, New York, p 2344

    Google Scholar 

  • Shanmugam V, Atri K, Gupta S, Kanoujia N, Naruka D (2011) Selection and differentiation of Bacillus spp. antagonistic to Fusarium oxysporum f.sp. lycopersici and Alternaria solani infecting tomato. Folia Microbiologica 56:170–177

    CAS  PubMed  Google Scholar 

  • Slifkin M (2000) Tween 80 Opacity Test Responses of Various Candida Species. Journal of Clinical Microbiology 38:4626–4628

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Molecular Microbiology 56:845–857

    CAS  PubMed  Google Scholar 

  • Sundaramoorthy S, Balabaskar P (2013) Biocontrol efficacy of Trichoderma spp. against wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici. Journal of Applied Biology Biotechnology 1:036–040

    Google Scholar 

  • Urrea R, Cabezas L, Sierra R, Cárdenas M, Restrepo S, Jiménez P (2011) Selection of antagonistic bacteria isolated from the Physalis peruviana rhizosphere against Fusarium oxysporum. Journal of Applied Microbiology 111:707–716

    CAS  PubMed  Google Scholar 

  • Valdenegro M, Almonacid S, Henríquez C, Lutz M, Fuentes L, Simpson R (2013) The effects of drying processes on organoleptic characteristics and the health quality of food ingredients obtained from goldenberry fruits (Physalis peruviana). Open Access Scientific Reports 2:642

    Google Scholar 

  • Vargas A, Correa A, Lozano DC, González A, Bernal A, Restrepo S (2007) First Report of Late Blight Caused by Phytophthora infestans on Cape Gooseberry (Physalis peruviana) in Colombia. Plant Disease Res 91:464

    CAS  Google Scholar 

  • Weber OB, Muniz CR, Vitor A, Freire F, Oliveira VM (2007) Interaction of endophytic diazotrophic bacteria and Fusarium oxysporum f. sp. cubense on plantlets of banana ‘Maça’. European Journal of Plant Pathology 298:47–56

    CAS  Google Scholar 

  • Xu X, Jeffries P, Pautasso M, Jeger M (2011) Combined use of biocontrol agents to manage plant diseases in theory and practice. Phytopathology 101:1024–1031

    CAS  PubMed  Google Scholar 

  • Zhang N, Yang D, Kendall J, Borriss R, Druzhinina I, Kubicek C, Shen Q, Zhang R (2016) Comparative genomic analysis of Bacillus amyloliquefaciens and Bacillus subtilis reveals evolutional traits for adaptation to plant-associated habitats. Frontiers in Microbiology 7:2039

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We would like to thank the Departamento de Ciencia, Tecnología e Innovación (COLCIENCIAS) and the Dirección de Investigaciones of the Universidad Pedagógica y Tecnológica de Colombia for funding and the young researcher scholarship internship for accomplishing the first stage of this project. We thank Asociación de Productores de Ciénega (ASOPROCIEN) and Agricultural engineer Fernando Becerra for sampling and Dr. Fernando Rodríguez for the molecular identification of some bacterial isolates.

Author information

Authors and Affiliations

  1. Universidad Nacional de Colombia, Bogotá, Colombia

    Deisy Lisseth Toloza-Moreno

  2. Universidad Pedagógica y Tecnológica de Colombia, Tunja, Colombia

    Deisy Lisseth Toloza-Moreno & Luz Marina Lizarazo-Forero

  3. Biotechnology Institute, Universidad Nacional de Colombia, A. A. 14-490, Bogotá, D. C, Colombia

    Daniel Uribe-Vélez

Authors
  1. Deisy Lisseth Toloza-Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luz Marina Lizarazo-Forero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel Uribe-Vélez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deisy Lisseth Toloza-Moreno.

Additional information

Section Editor: Marc Bardin

Publisher’s note

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

Electronic supplementary material

Supplementary Figure 1

Disease severity in terms of area under the disease of progress curve (AUDPC) of antagonistic activity of selected bacterial isolates against F. oxysporum (Fox17) under greenhouse conditions after 35 days of inoculation of cape gooseberry plants. The antagonist bacteria groups are show according to Fig. 4 a, b, c, d). G1: Composed by Bacillus sp. MB015, E. amnigenus MB068 and Providencia sp. MB106, G2 composed by Pseudomonas sp. MB108 and B. licheniformis MB109, G3: Bacteria of G1 and G2. C_Pos: BCA Control Ps. fluorescens IBUN Pfl 107. C. Abs: Absolute control (plants without pathogen or bacterial treatment). C + Fox17: Disease control with F. oxysporum´ strain Fox17. Tukey’s range test was applied with all treatments. Treatments with different letters show statistically significant differences (p < 0.05). (JPG 237 kb)

Supplementary Figure 2

Disease severity in terms of Area under the disease of progress curve (AUDPC) of antagonistic activity of selected bacterial isolates against F. oxysporum (Fox17) under greenhouse conditions after 28 days of inoculation of cape gooseberry plants. The antagonist bacteria groups are show according to Fig. 4 (4a, 4b, 4c, 4d). G1: Composed of Bacillus sp. MB015, E. amnigenus MB068 and Providencia sp. MB106, G2 composed of Pseudomonas sp. MB108 and B. licheniformis MB109, G3: Bacteria of G1 and G2. C_Pos: BCA Control Ps. fluorescens IBUN Pfl 107. C. Abs: Absolute control (plants without pathogen or bacterial treatment). C + Fox17: Disease control with F. oxysporum´ strain Fox17. Tukey’s range test was applied with all treatments. Treatments with different letters show statistically significant differences (p < 0.05). (JPG 232 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Toloza-Moreno, D.L., Lizarazo-Forero, L.M. & Uribe-Vélez, D. Antagonist capacity of bacteria isolated from cape gooseberry cultures (Physalis peruviana L.) for biological control of Fusarium oxysporum. Trop. plant pathol. 45, 1–12 (2020). https://doi.org/10.1007/s40858-019-00313-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40858-019-00313-z

Keywords

Search

Navigation