Skip to main content
SpringerLink
Log in

Evaluation of antagonistic activity and mechanisms of endophytic yeasts against pathogenic fungi causing economic crop diseases

  • Original Article
  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

This work aimed to evaluate in vitro antagonistic activities and mechanisms of endophytic yeasts against phytopathogenic fungi. A total of 407 yeast strains isolated from tissue of rice, corn, and sugarcane leaves were evaluated for their antagonistic activities against ten phytopathogenic fungi. Only strains of Wickerhamomyces anomalus and Kodamaea ohmeri were found to inhibit the growth of phytopathogenic fungi. Wickerhamomyces anomalus (seven strains) showed antagonistic activity against Curvularia lunata (cause of dirty panicle disease of rice), three Fusarium moniliforme strains (cause of bakanae disease of rice, stalk rot disease of corn, and red rot disease of sugarcane), and Rhizoctonia solani (cause of sheath blight disease of rice). Whereas four Kodamae ohmeri strains inhibited growth of F. moniliforme (cause of bakanae disease of rice). Antagonistic mechanisms of W. anomalus were based on the production of volatile organic compounds (VOCs) (mainly 3-methyl-1-butyl acetate and 3-methyl-1-butanol), fungal cell wall-degrading enzymes (β-1,3-glucanase and chitinase), and siderophores as well as phosphate and zinc oxide solubilization. As for K. ohmeri, the production of VOCs (mainly 3-methyl-1-butanol), β-1,3-glucanase and chitinase were hypothesized as possible mechanisms. The antagonistic activity of W. anomalus against these phytopathogenic fungi and of K. ohmeri against F. moniliforme, and the analysis of the VOCs produced by K. ohmeri are reported for the first time. Two W. anomalus strains, DMKU-RE13 and DMKU-CE52, were evaluated for controlling rice sheath blight disease caused by R. solani in rice plants in the greenhouse and found to suppress the disease 55.2–65.1%, whereas 3% validamycin suppressed this disease by 88.5%.

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
Fig. 5

Similar content being viewed by others

References

  • Ando H, Hatanaka K, Ohata I, Yamashita-Kitaguchi Y, Kurata A, Kishimoto N (2012) Antifungal activities of volatile substances generated by yeast isolated from Iranian commercial cheese. Food Control 26:472–478

    Article  CAS  Google Scholar 

  • Azevedo JL, Jr WM, Pereira JO, de Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:1–4

    Article  Google Scholar 

  • Calvente V, Benuzzi D, Sanz de Tosetti MI (1999) Antagonistic action of siderophores from Rhodotorula glutinis upon the postharvest pathogen Penicillium expansum. Int Biodeterior Biodegradation 43:167–172

    Article  CAS  Google Scholar 

  • Cheng Y, Hong T, Liu C, Meng M (2009) Cloning and functional characterization of a complex endo-β-1,3-glucanase from Paenibacillus sp. Appl Microbiol Biotechnol 1:1051–1061

    Article  CAS  Google Scholar 

  • Coelho AR, Celli MG, Ono EYS, Wosiacki G, Hoffmann FL, Pagnocca FC, Hirooka YE (2007) Penicillium expansum versus antagonist yeasts and patulin degradation in vitro. Braz Arch Biol Technol 50:725–733

    Article  Google Scholar 

  • Droby S, Wisniewski M, Macarisin D, Wilson C (2009) Twenty years of postharvest biocontrol research: is it time for a new paradigm? Postharvest Biol Technol 52:137–145

    Article  Google Scholar 

  • Druvefors U, Passoth V, Schnürer J (2005) Nutrient effects on biocontrol of Penicillium roqueforti by Pichia anomala J121 during airtight storage of wheat. Appl Environ Microbiol 71:1865–1869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garrido CC, Usall J, Torres R, Teixidó N (2017) Effective control of Botrytis bunch rot in commercial vineyards by large-scale application of Candida sake CPA-1. BioControl 62:161–173

    Article  Google Scholar 

  • Giobbe S, Marceddu S, Scherm B, Zara G, Mazzarello VL, Budroni M, Migheli Q (2007) The strange case of a biofilm-forming strain of Pichia fermentans, which controls Monilinia brown rot on apple but is pathogenic on peach fruit. FEMS Yeast Res 7:1389–1398

    Article  CAS  PubMed  Google Scholar 

  • Hua SST, Beck JJ, Sarreal SBL, Gee W (2014) The major volatile compound 2-phenylethanol from the biocontrol yeast, Pichia anomala, inhibits growth and expression of aflatoxin biosynthetic genes of Aspergillus flavus. Mycotoxin Res 30:71–78

    Article  CAS  PubMed  Google Scholar 

  • Huang R, Li GQ, Zhang J, Yang L, Che HJ, Jiang DH, Huang HC (2011) Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology 101:859–869

    Article  CAS  PubMed  Google Scholar 

  • Huang R, Che HJ, Zhang J, Yang L, Jiang DH, Li GQ (2012) Evaluation of Sporidiobolus pararoseus strain YCXT3 as biocontrol agent of Botrytis cinerea on post-harvest strawberry fruits. Biol Control 62:53–63

    Article  Google Scholar 

  • Jamalizadeh M, Etebarian HR, Aminian H, Alizadeh A (2011) A review of mechanisms of action of biological control organisms against post-harvest fruit spoilage. Bull OEPP/EPPO Bull 41:65–71

    Article  Google Scholar 

  • Jayaprakashvel M, Selvakumar M, Srinivasan K, Ramesh S, Mathivanan N (2010) Control of sheath blight disease in rice by thermostable secondary metabolites of Trichoderma roseum MML003. Eur J Plant Pathol 126:229–239

    Article  Google Scholar 

  • Jayaswal RK, Fernandez M, Upadhyay RS, Visintin L, Kurz M, Webb J, Rinehart K (1993) Antagonism of Pseudomonas cepacia against phytopathogenic fungi. Curr Microbiol 26:17–22

    Article  CAS  PubMed  Google Scholar 

  • Khunnamwong P, Jindamorakot S, Limtong S (2018) Endophytic yeasts diversity in leaf tissue of rice, corn and sugarcane cultivated in Thailand assessed by a culture-dependent approach. Fungal Biol 122:1–5

    Article  Google Scholar 

  • Kunyosying D, To-anun C, Cheewangkoon R (2018) Control of rice blast disease using antagonistic yeasts. Int J Agric Technol 14:83–98

    CAS  Google Scholar 

  • Leksomboon C, Lertsrutaiyotin R (2014) Evaluation of red rot disease resistance in sugarcane varieties Kamphaeng Sean. In proceedings of the 52nd Kasetsart University Annual Conference, p 329–333

  • Linnakoski R, Puhakka-Tarvainen H, Pappinen A (2012) Endophytic fungi isolated from Khaya anthotheca in Ghana. Fungal Ecol 5:298–308

    Article  Google Scholar 

  • Marcello CM, Steindorff AS, Silva SP, Silva RN, Bataus LAM, Ulhoa CJ (2010) Expression analysis of the exo-β-1,3-glucanase from the mycoparasitic fungus Trichoderma asperellum. Microbiol Res 165:75–81

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S (2014) Plant growth-promoting traits of epiphytic and endophytic yeasts isolated from rice and sugar cane leaves in Thailand. Fungal Biol 118:683–694

    Article  CAS  PubMed  Google Scholar 

  • Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oro L, Feliziani E, Ciania M, Romanazzib G, Comitinia F (2018) Volatile organic compounds from Wickerhamomyces anomalus, Metschnikowia pulcherrima and Saccharomyces cerevisiae inhibit growth of decay causing fungi and control postharvest diseases of strawberries. Int J Food Microbiol 265:18–22

    Article  CAS  PubMed  Google Scholar 

  • Pal KK, Tilak KVBR, Saxena AK, Dey R, Singh CS (2001) Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria. Microbiol Res 156:209–223

    Article  CAS  PubMed  Google Scholar 

  • Parafati L, Vitale A, Restuccia C, Cirvilleri G (2015) Biocontrol ability and action mechanism of food-isolated yeast strains against Botrytis cinerea causing post-harvest bunch rot of table grape. Food Microbiol 47:85–92

    Article  CAS  PubMed  Google Scholar 

  • Park D, Sayler R, Hong Y, Nam M, Yang Y (2008) A method for inoculation and evaluation of rice sheath blight disease. Plant Dis 92:25–29

    Article  PubMed  Google Scholar 

  • Plodpai P, Chuenchitt S, Petcharat V, Chakthong S, Voravuthikunchai SP (2013) Anti-Rhizoctonia solani activity by Desmos chinensis extracts and its mechanism of action. Crop Prot 43:65–71

    Article  Google Scholar 

  • Prasongsuk S, Lotrakul P, Ali I, Bankeeree W, Punnapayak H (2018) The current status of Aureobasidium pullulans in biotechnology. Folia Microbiol 63:129–140

    Article  CAS  Google Scholar 

  • Rice Department, Ministry of Agriculture and Cooperatives of Thailand (2014) Rice knowledge bank. http://www.ricethailand.go.th/rkb3/Disease.htm. Accessed 2 Nov 2019

  • Rokhbakhsh-Zamin F, Sachdev D, Kazemi-Pour N, Engineer A, Pardesi KR, Zinjarde S, Dhakephalka PK, Chopade BA (2011) Characterization of plant-growth-promoting traits of Acinetobacter species isolated from rhizosphere of Pennisetum glaucum. J Microbiol Biotechnol 21:556–566

    Article  PubMed  CAS  Google Scholar 

  • Rosa MM, Tauk-Tornisielo SM, Rampazzo PE, Ceccato-Antonini SR (2010) Evaluation of the biological control by the yeast Torulaspora globosa against Colletotrichum sublineolum in sorghum. World J Microbiol Biotechnol 26:1491–1502

    Article  Google Scholar 

  • Ruzicka F, Holá V, Votava M, Tejkalová R (2007) Importance of biofilm in Candida parapsilosis and evaluation of its susceptibility to antifungal agents by colorimetric method. Folia Microbiol 52:209–214

    Article  CAS  Google Scholar 

  • Sangdit P, Leksomboon C, Lertsrutaiyotin R (2014) Cultural, morphological and pathological characterization of Colletotrichum falcatum causing red rot disease of sugarcane in Thailand. Kasetsart J (Nat Sci) 48:880–892

    Google Scholar 

  • Saravanakumar D, Spadaro D, Garibaldi A, Gullino ML (2009) Detection of enzymatic activity and partial sequence of a chitinase gene in Metschnikowia pulcherrima strain MACH1 used as post-harvest biocontrol agent. Eur J Plant Pathol 123:183–193

    Article  CAS  Google Scholar 

  • Schisler DA, Core AB, Boehm MJ, Horst L, Krause C, Dunlap CA, Rooney AP (2014) Population dynamics of the Fusarium head blight biocontrol agent Cryptococcus flavescens OH 182.9 on wheat anthers and heads. Biol Control 70:17–27

    Article  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Sisti M, Savini V (2014) Antifungal properties of the human Metschnikowia strain IHEM 25107. Folia Microbiol 59:263–266

    Article  CAS  Google Scholar 

  • Sobek EA, Munkvold GP (1999) European corn borer (Lepidoptera: Pyralidae) larvae as vectors of Fusarium moniliforme, causing kernel rot and symptomless infection of maize kernels. J Econ Entomol 92:503–509

    Article  Google Scholar 

  • Spadaro D, Droby S (2016) Development of biocontrol products for postharvest diseases of fruit: the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food Sci Technol 47:39–49

    Article  CAS  Google Scholar 

  • Spadaro D, Vola R, Piano S, Gullino ML (2002) Mechanisms of action and efficacy of four isolates of the yeast Metschnikowia pulcherrima active against postharvest pathogens on apples. Postharvest Biol Technol 24:123–134

    Article  Google Scholar 

  • Spadaro D, Ciavorella A, Zhang D, Garibaldi A, Gullino ML (2010) Effect of culture media and pH on the biomass production and biocontrol efficacy of a Metschnikowia pulcherrima strain to be used as a biofungicide for postharvest disease control. Can J Microbiol 56:128–137

    Article  CAS  PubMed  Google Scholar 

  • Suwannarach N, Kaewyana C, Yodmeeklin A, Kumla J, Matsui K, Lumyong S (2017) Evaluation of Muscodor cinnamomi as an egg biofumigant for the reduction of microorganisms on eggshell surfaces and its effect on egg quality. Int J Food Microbiol 244:52–61

    Article  CAS  PubMed  Google Scholar 

  • Vero S, Garmendia G, González MB, Bentancur O, Wisniewski M (2013) Evaluation of yeasts obtained from Antarctic soil samples as biocontrol agents for the management of postharvest diseases of apple (Malus×domestica). FEMS Yeast Res 13:189–199

    Article  CAS  PubMed  Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997

    Article  CAS  PubMed  Google Scholar 

  • Zepeda-Giraud LF, Olicón-Hernandez DR, Martínez-López C, Guerra-Sánchez G (2016) Study of the action mode of Wickerhamomyces anomalus against Colletotrichum gloeosporioides. J Agric Sci Technol 6:341–349

    CAS  Google Scholar 

  • Zhang D, Spadaro D, Garibaldi A, Gullino ML (2010) Efficacy of the antagonist Aureobasidium pullulans PL5 against postharvest pathogens of peach, apple and plum and its modes of action. Biol Control 54:172–180

    Article  Google Scholar 

  • Zhou Y, Li W, Zeng J, Shao Y (2018) Mechanisms of action of the yeast Debaryomyces nepalensis for control of the pathogen Colletotrichum gloeosporioides in mango fruit. Biol Control 123:111–119

    Article  CAS  Google Scholar 

  • Ziedan EHE, Farrag ESH (2011) Application of yeasts as biocontrol agents for controlling foliar diseases on sugar beet plants. J Agric Sci Technol 7:1789–1799

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank Asst. Prof. Dr.Onuma Piasai, Department of Plant Pathology, Faculty of Agriculture, Kasetsart University for providing Fusarium moniliforme, cause of red and stem rot in sugarcane plant.

Funding

This work was supported by the Thailand Research Fund through the TRF Research-Team Promotion Grant (RTA5480009 and RTA6080004) and the Royal Golden Jubilee Ph.D. program grant no. PHD/0128/2554.

Author information

Author notes

  1. Pannida Khunnamwong

    Present address: Department of Food Technology, Faculty of Engineering and Industrial Technology, Silpakorn University, Sanamchandra Palace Campus, Nakhon Pathom, 73000, Thailand

Authors and Affiliations

  1. Department of Microbiology, Faculty of Science, Kasetsart University, Bangkok, 10900, Thailand

    Pannida Khunnamwong, Noppon Lertwattanasakul & Savitree Limtong

  2. National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathum Thani, 12120, Thailand

    Sasitorn Jindamorakot

  3. Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand

    Nakarin Suwannarach

  4. Department of Applied Molecular Bioscience, Graduate School of Medicine and Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, 753-8515, Japan

    Kenji Matsui

  5. Academy of Science, Royal Society of Thailand, Bangkok, 10300, Thailand

    Savitree Limtong

Authors
  1. Pannida Khunnamwong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Noppon Lertwattanasakul
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sasitorn Jindamorakot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nakarin Suwannarach
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kenji Matsui
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Savitree Limtong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Pannida Khunnamwong performed experiments, analyzed data, and wrote the manuscript. Noppon Lertwattanasakul edited the manuscript. Sasitorn Jindamorakot edited the manuscript. Nakarin Suwannarach performed VOCs analysis and analyzed VOCs data. Kenji Matsui recommendation on volatile analysis experiment and edited the manuscript. Savitree Limtong designed study, discussed data, and edited the manuscript.

Corresponding author

Correspondence to Savitree Limtong.

Ethics declarations

Conflict of interest

The 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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khunnamwong, P., Lertwattanasakul, N., Jindamorakot, S. et al. Evaluation of antagonistic activity and mechanisms of endophytic yeasts against pathogenic fungi causing economic crop diseases. Folia Microbiol 65, 573–590 (2020). https://doi.org/10.1007/s12223-019-00764-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-019-00764-6

Search

Navigation