Skip to main content

Advertisement

Log in

The efficacy of Iranian Pythium oligandrum isolates in biocontrol of soil-borne fungal pathogens of tomato

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

Abstract

Pythium oligandrum is known as an important biological control agent against fungal plant pathogens. The commercial formulations of this oomycete could reduce the application of the chemical fungicides and lessen the environmental impact of treatments. This study aimed to investigate the antagonistic ability of Iranian isolates of P. oligandrum to select proper and efficient candidates as native biocontrol agents using a previously characterized collection of forty-five isolates from fields of different regions of Iran. The antagonistic effects of native P. oligandrum isolates were evaluated against two soil-borne fungal pathogens, Fusarium oxysporum f. sp. lycopersici and Phytophthora parasitica, causing diseases on tomato. Pythium oligandrum isolates K29, K48, and K87 were recognized as the most effective isolates based also on previously published in vitro antagonistic assays, oligandrin production, and the ability of root colonization. The oospores of the selected candidates were formulated as seed-coating, kaolin dust mixture, and perlite-coating and compared with common fungicides in greenhouse tests. The results of greenhouse studies revealed that all selected P. oligandrum isolates and chemical fungicides significantly reduced disease severity but the efficacy of P. oligandrum isolates varied according to the type of formulation. Seed-coating formulation with oospores exhibited better performance than other formulations. The results showed that the application of formulated P. oligandrum selected isolates had the same performance (40–50% reduction in disease severity) as compared to the chemical fungicide treatments for controlling soil-borne pathogens. These results make it possible to consider in the near future the use of isolates of P. oligandrum as biocontrol agents to protect vegetable crops, in particular tomato, from soil-borne pathogens.

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

Similar content being viewed by others

References

  • Abbasi S, Safaie N, Sadeghi A, Shamsbakhsh M (2019) Streptomyces strains induce resistance to Fusarium oxysporum f. sp. lycopersici race 3 in tomato through different molecular mechanisms. Front Microbiol 10:1505

  • Aimé S, Alabouvette C, Steinberg C, Olivain C (2013) The endophytic strain Fusarium oxysporum Fo47: a good candidate for priming the defense responses in tomato roots. Mol Plant-Microbe Interact 26:918–926

    PubMed  Google Scholar 

  • Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situation. Eur J Plant Pathol 114:329–341

  • Al-Hamdani AM, Cooke RC (1983) Effects of the mycoparasite Pythium oligandrum on cellulolysis and sclerotium production by Rhizoctonia solani. Trans Br Mycol Soc 81:619–621

    Google Scholar 

  • Al-Rawahi AK, Hancock JG (1998) Parasitism and biological control of Verticillium dahliae by Pythium oligandrum. Plant Dis 82:1100–1106

    CAS  PubMed  Google Scholar 

  • Arie T, Takahashi H, Kodama M, Teraoka T (2007) Tomato as a model plant for plant-pathogen interactions. Plant Biotechnol 24:135–147

    CAS  Google Scholar 

  • Ashrafizadeh A, Etebarian HR, Zamanizadeh HR (2005) Evaluation of Trichoderma isolates for biocontrol of Fusarium wilt of melon. Iran J Plant Pathol 41:39–57

    Google Scholar 

  • Benhamou N, Bélanger RR, Rey P, Tirilly Y (2001) Oligandrin, the elicitin-like protein produced by the mycoparasite Pythium oligandrum, induces systemic resistance to Fusarium crown and root rot in tomato plants. Plant Physiol Biochem 39:681–696

    CAS  Google Scholar 

  • Benhamou N, Le Floch G, Vallance J, Gerbore J, Grizard D, Rey P (2012) Pythium oligandrum: an example of opportunistic success. Microbiology 158:2679–2694

    CAS  PubMed  Google Scholar 

  • Bonnet P, Bourdon E, Ponchet M, Blein JP, Ricci P (1996) Acquired resistance triggered by elicitins in tobacco and other plants. Eur J Plant Pathol 102:181–192

    CAS  Google Scholar 

  • Brožová JANA (2002) Exploitation of the mycoparasitic fungus Pythium oligandrum in plant protection. Plant Prot Sci 38:29–35

    Google Scholar 

  • Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25:1327–1333

    CAS  PubMed  Google Scholar 

  • Daly P, Chen S, Xue T, Li J, Sheikh TMM, Zhang Q, Wang X, Zhang J, Fitzpatrick DA, McGowan J, Dezng S, Jiu M, Zhou D, Druzhininia IS, Wei L (2021) Dual-Transcriptomic, Microscopic, and Biocontrol Analyses of the Interaction Between the Bioeffector Pythium oligandrum and the Pythium Soft-Rot of Ginger Pathogen Pythium myriotylum. Front Microbiol 12:765872–765872

    PubMed  PubMed Central  Google Scholar 

  • Daraignes L, Gerbore J, Yacoub A, Dubois L, Romand C, Zekri O, Roudet J, Chambon P, Fermaud M (2018) Efficacy of Pythium oligandrum affected by its association with bacterial BCAs and rootstock effect in controlling grapevine trunk diseases. Biol Control 119:59–67

    Google Scholar 

  • Erika C, Griebel S, Naumann M, Pawelzik E (2020) Biodiversity in tomatoes: Is it reflected in nutrient density and nutritional yields under organic outdoor production? Front Plant Sci 11:589692

    PubMed  PubMed Central  Google Scholar 

  • FAOSTAT (2020) Statistics, Food and Agriculture Organization of the United Nations, Rome

  • Farrokhi F, Hajian shahri M, Salari M, Rohani H (2014) Evaluation of some antagonistic aspects of Pythium oligandrum (Dresch) for biological control of Rhizoctonia solani (Kuhn), the causal agent of sugar beet damping-off in laboratory. Res Plant Pathol 2:51–70

  • Ferrero V, Baeten L, Blanco-Sánchez L, Planelló R, Díaz-Pendón JA, Rodríguez-Echeverría S, de la Peña E (2020) Complex patterns in tolerance and resistance to pests and diseases underpin the domestication of tomato. New Phytol 226:254–266

    PubMed  Google Scholar 

  • Gawai DU (2018) Role of Fungi as biocontrol agents for the control of plant diseases in sustainable agriculture. In: Fungi and their Role in Sustainable Development: Current Perspectives. Springer, Singapore, pp 283–291

  • Gerbore J, Benhamou N, Vallance J, Le Floch G, Grizard D, Regnault-Roger C, Rey P (2014a) Biological control of plant pathogens: advantages and limitations seen through the case study of Pythium oligandrum. Environ Sci Pollut Res Int 21:4847–4860

    CAS  PubMed  Google Scholar 

  • Gerbore J, Vallance J, Yacoub A, Delmotte F, Grizard D, Regnault-Roger C, Rey P (2014b) Characterization of Pythium oligandrum populations that colonize the rhizosphere of vines from the Bordeaux region. FEMS Microbiol Ecol 90:153–167

    CAS  PubMed  Google Scholar 

  • Giotis Ch, Markelou E, Theodoropoulou A, Toufexi E, Hodson R, Shotton P, Shiel R, Cooper J, Leifert C (2009) Effect of soil amendments and biological control agents (BCAs) on soil-borne root diseases caused by Pyrenochaeta lycopersici and Verticillium albo-atrum in organic greenhouse tomato production systems. Eur J Plant Pathol 123:387–400

  • Gramaje D, Urbez-Torres JR, Sosnowski MR (2018) Managing grapevine trunk diseases with respect to etiology and epidemiology: current strategies and future prospects. Plant Dis 102:12–39

    PubMed  Google Scholar 

  • Haghi Z, Mostowfizadeh-Ghalamfarsa R, Edel-Hermann V (2020a) Genetic diversity of Pythium oligandrum in Iran. J Plant Pathol 102:1197–1204

    Google Scholar 

  • Haghi Z, Mostowfizadeh-Ghalamfarsa R, Hamzehzarghani H (2020b) Identification, distribution and functional diversity of Iranian isolates of Pythium oligandrum. BioControl Plant Prot 7:91–112

  • He SS, Zhang BX, Ge QX (1992) On the antagonism by hyperparasite Pythium oligandrum. Acta Phytopathol Sin 22:77–82

    Google Scholar 

  • Houshyar E, Dalgaard T, Tarazkar MH, Jørgensen U (2015) Energy input for tomato production what economy says, and what is good for the environment. J Clean Prod 89:99–109

    Google Scholar 

  • Ikeda S, Shimizu A, Shimizu M, Takahashi H, Takenaka S (2012) Biocontrol of black scurf on potato by seed tuber treatment with Pythium oligandrum. Biol Control 60:297–304

    Google Scholar 

  • Karthika S, Varghese S, Jisha MS (2020) Exploring the efficacy of antagonistic rhizobacteria as native biocontrol agents against tomato plant diseases. 3 Biotech 10:1–17

  • La Spada F, Stracquadanio C, Riolo M, Pane A, Cacciola SO (2020) Trichoderma counteracts the challenge of Phytophthora nicotianae Infections on tomato by modulating plant defense mechanisms and the expression of crinkler, necrosis-inducing Phytophthora protein 1, and cellulose-binding elicitor lectin pathogenic effectors. Front Plant Sci 11:583539

    PubMed  PubMed Central  Google Scholar 

  • Larousse M, Galiana E (2017) Microbial partnerships of pathogenic oomycetes. PLoS Pathog 13:e1006028

    PubMed  PubMed Central  Google Scholar 

  • Le Floch G, Benhamou N, Mamaca E, Salerno MI, Tirilly Y, Rey P (2005) Characterisation of the early events in atypical tomato root colonisation by a biocontrol agent, Pythium oligandrum. Plant Physiol Biochem 43:1–11

    PubMed  Google Scholar 

  • Le Floch G, Rey P, Déniel F, Benhamou N, Picard K, Tirilly Y (2003) Enhancement of development and induction of resistance in tomato plants by the antagonist, Pythium oligandrum. Agronomie 23:455–460

    Google Scholar 

  • Le Floch G, Vallance J, Benhamou N, Rey P (2009) Combining the oomycete Pythium oligandrum with two other antagonistic fungi: root relationships and tomato grey mold biocontrol. Biol Control 50:288–298

    Google Scholar 

  • Lherminier J, Benhamou N, Larrue J, Milat ML, Boudon-Padieu E, Nicole M, Blein JP (2003) Cytological characterization of elicitin-induced protection in tobacco plants infected by Phytophthora parasitica or Phytoplasma. Phytopathology 93:1308–1319

    CAS  PubMed  Google Scholar 

  • Lou B, Wang A, Lin C, Xu T, Zheng X (2011) Enhancement of defense responses by oligandrin against Botrytis cinerea in tomatoes. Afr J Biotechnol 10:11442–11449

    CAS  Google Scholar 

  • Martin FN, Hancock JG (1986) Association of chemical and biological factors in soils suppressive to Pythium ultimum. Phytopathology 76:1221–1231

    CAS  Google Scholar 

  • Massumi H, Shaabanian M, Pour AH, Heydarnejad J, Rahimian H (2009) Incidence of viruses infecting tomato and their natural hosts in the southeast and central regions of Iran. Plant Dis 93:67–72

    CAS  PubMed  Google Scholar 

  • Masunaka A, Sekiguchi H, Takahashi H, Takenaka S (2010) Distribution and expression of elicitin-like protein genes of the biocontrol agent Pythium oligandrum. J Phytopathol 158:417–426

    CAS  Google Scholar 

  • McGovern RJ (2015) Management of tomato diseases caused by Fusarium oxysporum. Crop Prot 73:78–92

    Google Scholar 

  • McQuilken MP, Whipps JM, Cooke RC (1990) Oospores of the biocontrol agent Pythium oligandrum bulk-produced in liquid culture. Mycol Res 94:613–616

    Google Scholar 

  • Mirsoleimani Z, Mostowfizadeh-Ghalamfarsa R (2013) Characterization of Phytophthora pistaciae, the causal agent of pistachio gummosis, based on host range, morphology, and ribosomal genome. Phytopathol Mediterr 52:501–516

    Google Scholar 

  • Mohamed N, Lherminier J, Farmer MJ, Fromentin J, Béno N, Houot V, Milat ML, Blein JP (2007) Defense responses in grapevine leaves against Botrytis cinerea induced by application of a Pythium oligandrum strain or its elicitin, oligandrin, to roots. Phytopathology 97:611–620

    CAS  PubMed  Google Scholar 

  • Mondello V, Songy A, Battiston E, Pinto C, Coppin C, Trotel-Aziz P, Clement C, Mugnai L, Fontaine F (2018) Grapevine trunk diseases: a review of fifteen years of trials for their control with chemicals and biocontrol agents. Plant Dis 102:1189–1217

    CAS  PubMed  Google Scholar 

  • Ng CA, Pernica M, Yap J, Belakova S, Vaculova K, Branyik T (2021) Biocontrol effect of Pythium oligandrum on artificial Fusarium culmorum infection during malting of wheat. J Cereal Sci 100:6

    Google Scholar 

  • Olowe OM, Nicola L, Asemoloye MD, Akanmu AO, Babalola OO (2022) Trichoderma: Potential bio-resource for the management of tomato root rot diseases in Africa. Microbiol Res 257:126978

    CAS  PubMed  Google Scholar 

  • Ouyang Z, Li X, Huang L, Hong Y, Zhang Y, Zhang H, Li D, Song F (2015) Elicitin-like proteins Oli-D1 and Oli-D2 from Pythium oligandrum trigger hypersensitive response in Nicotiana benthamiana and induce resistance against Botrytis cinerea in tomato. Mol Plant Pathol 16:238–250

    CAS  PubMed  Google Scholar 

  • Picard K, Ponchet M, Blein JP, Rey P, Tirilly Y, Benhamou N (2000a) Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrum induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiol 124:379–396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Picard K, Tirilly Y, Benhamou N (2000b) Cytological effects of cellulases in the parasitism of Phytophthora parasitica by Pythium oligandrum. Appl Environ Microbiol 66:4305–4314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pirayesh S, Zamanizade H, Morid B (2018) Molecular Identification of Physiological Races of Fusarium oxysporum f. sp. lycopersici and radicis lycopersici Causal Agent of Fusarium Wilt of Tomato in Iran. J Agric Sci Technol 20:193–202

    Google Scholar 

  • Pishgar-Komleh SH, Akram A, Keyhani A, Sefeedpari P, Shine P, Brandao M (2020) Integration of life cycle assessment, artificial neural networks, and metaheuristic optimization algorithms for optimization of tomato-based cropping systems in Iran. LTWA 25:620–632

    CAS  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 37:202–212

    PubMed  Google Scholar 

  • Rey P, Le Floch G, Benhamou N, Tirilly Y (2008) Pythium oligandrum biocontrol: Its relationships with fungi and plants. Plant Microbe Interact 37:43–57

    Google Scholar 

  • Rey P, Picard K, Déniel F, Benhamou N, Tirilly Y (1999) Development an IPM system in soilless culture by using slow filtration and a biocontrol fungus, Pythium oligandrum. IOBC WPRS Bulletin (France)

  • Satková P, Starý T, Plešková V, Zapletalová M, Kašparovský T, Činčalová-Kubienová L, Petřivalský M (2017) Diverse responses of wild and cultivated tomato to BABA, oligandrin and Oidium neolycopersici infection. Ann Bot 119:829–840

    PubMed  Google Scholar 

  • Snapp SS, Shennan C, Van Bruggen AHC (1991) Effects of salinity on severity of infection by Phytophthora parasitica Dast., ion concentrations and growth of tomato Lycopersicon Esculentum. Mill New Phytol 119:275–284

    CAS  PubMed  Google Scholar 

  • Song W, Zhou L, Yang C, Cao X, Zhang L, Liu X (2004) Tomato Fusarium wilt and its chemical control strategies in a hydroponic system. Crop Prot 23:243–247

    CAS  Google Scholar 

  • Takenaka S (2015) Studies on biological control mechanisms of Pythium oligandrum. J Gen Plant Pathol 81:466–469

    Google Scholar 

  • Takenaka S, Sekiguchi H, Nakaho K, Tojo M, Masunaka A, Takahashi H (2008) Colonization of Pythium oligandrum in the tomato rhizosphere for biological control of bacterial wilt disease analyzed by real-time PCR and confocal laser-scanning microscopy. Phytopathology 98:187–195

    CAS  PubMed  Google Scholar 

  • Vos CM, Yang Y, De Coninck B, Cammue BPA (2014) Fungal (-like) biocontrol organisms in tomato disease control. Biol Control 74:65–81

    Google Scholar 

  • Wan A, Lou B, Xu T, Lin C (2011) Defense responses in tomato fruit induced by oligandrin against Botrytis cinerea. Afr J Biotechnol 10:4596–4601

    Google Scholar 

  • Wulff EG, Pham ATH, Chérif M, Rey P, Tirilly Y, Hockenhull J (1998) Inoculation of cucumber roots with zoospores of mycoparasitic and plant pathogenic Pythium species: differential zoospore accumulation, colonization ability and plant growth response. Eur J Plant Pathol 104:69–76

    Google Scholar 

  • Yacoub A, Magnin N, Gerbore J, Haidar R, Bruez E, Compant S, Guyoneaud R, Rey P (2020) The biocontrol root-oomycete, Pythium oligandrum, triggers grapevine resistance and shifts in the transcriptome of the trunk pathogenic fungus Phaeomoniella Chlamydospora. Int J Mol Sci 21:6876

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang E, Li D, Yin P, Xie Q, Li Y, Lin Q, Duan Y (2021) A novel surface-enhanced Raman scattering (SERS) strategy for ultrasensitive detection of bacteria based on three-dimensional (3D) DNA walker. Biosens i 172:112758

    CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the Iran National Science Foundation (INSF, award number 96008191).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Reza Mostowfizadeh-Ghalamfarsa.

Ethics declarations

Ethical approval

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

Conflict of interest

All authors declare that they have no conflict of interest.

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 20 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Haghi, Z., Mostowfizadeh-Ghalamfarsa, R. & Steinberg, C. The efficacy of Iranian Pythium oligandrum isolates in biocontrol of soil-borne fungal pathogens of tomato. J Plant Pathol 105, 185–196 (2023). https://doi.org/10.1007/s42161-022-01245-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42161-022-01245-5

Keywords

Navigation