Skip to main content
Log in

Antagonism of Trichoderma-based biofungicides against Brazilian and North American isolates of Sclerotinia sclerotiorum and growth promotion of soybean

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The antagonistic activity of Trichoderma asperellum (aerial conidia) and T. harzianum (microsclerotia) Pers. (1801) (Hypocreales: Hypocreaceae) was evaluated against six isolates of Sclerotinia sclerotiorum (Lib.) de Bary (Helotiales: Sclerotiniaceae) from Brazil and the USA and further assessed for their enhancement of soybean growth. The fungicide thiophanate-methyl was included as a standard in all experiments. In vitro assay revealed that thiophanate-methyl and Trichoderma spp. effectively suppressed carpogenic and myceliogenic germination of sclerotia. The S. sclerotiorum isolates from Brazil appeared to be less susceptible than those from the USA to both chemical and biological treatments. The in vivo seed coating test using thiophanate-methyl or Trichoderma spp. substantially improved seed germination and suppressed growth of all S. sclerotiorum isolates to varying degrees. Moreover, soybean biomass of shoots and roots, and root nodulation were increased by either thiophanate-methyl or Trichoderma species. Collectively, these results underline the antagonistic activity of Trichoderma spp. against S. sclerotiorum isolates, the importance of Trichoderma spp. to improve soybean growth, and the bioactivity of Trichoderma microsclerotia through seed coating.

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.

Similar content being viewed by others

References

  • Abawi G, Grogan R (1979) Epidemiology of diseases caused by Sclerotinia species. Phytopathology 6:899–904

    Article  Google Scholar 

  • Abdullah M, Ali N, Suleman P (2008) Biological control of Sclerotinia sclerotiorum (Lib.) de Bary with Trichoderma harzianum and Bacillus amyloliquefaciens. Crop Prot 27:1354–1359

    Article  Google Scholar 

  • Ayoubi N, Zafari D, Mirabolfathy M (2012) Combination of Trichoderma species and Bradyrhizobium japonicum in control of Phytophthora sojae and soybean growth. J Crop Prot 1:67–79

    Google Scholar 

  • Bettiol W, Morandi MB (2009) Biocontrole de doenças de plantas: uso e perspectivas. Embrapa Meio Ambiente, Jaguariúna, p 341

    Google Scholar 

  • Chamberlain DW (1951) Sclerotinia stem rot of soybeans. Plant Dis Rep 35:490–491

    Google Scholar 

  • Contreras-Cornejo H, Ortiz-Castro R, López-Bucio J, Mukherjee PK (2013) Promotion of plant growth and induction of systemic defence by Trichoderma: physiology, genetics and gene expression. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M (eds) Trichoderma: biology and applications. CABI, Wallingford, pp 173–194

    Chapter  Google Scholar 

  • Contreras-Cornejo HA, Macías-Rodríguez L, del Val E, Larsen J (2016) Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol Ecol 92:36

    Article  CAS  Google Scholar 

  • Contreras-Cornejo HÁ, del Val E, Macía-Rodríguez L, Alarcón A, González-Esquivel C, Larsen J (2018a) Trichoderma atroviride, a maize root associated fungus, increases the parasitism rate of the fall armyworm Spodoptera frugiperda by its natural enemy Campoletis sonorensis. Soil Biol Biochem 122:196–202

    Article  CAS  Google Scholar 

  • Contreras-Cornejo HA, Macía-Rodríguez L, del Val E, Larsen J (2018b) The endophytic fungus Trichoderma atroviridae induces foliar herbivory resistance in maize plants. Appl Soil Ecol 124:45–53

    Article  Google Scholar 

  • Davidse LC (1986) Benzimidazole fungicides: mechanism of action and biological impact. Annu Rev Phytopathol 24:43–65

    Article  CAS  Google Scholar 

  • Donaldson PA, Anderson T, Lane BG, Davidson AL, Simmonds DH (2001) Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum. Physiol Mol Plant Pathol 59:297–307

    Article  CAS  Google Scholar 

  • Durman S, Menendez A, Godeas A (2005) Variation in oxalic acid production and mycelial compatibility within field populations of Sclerotinia sclerotiorum. Soil Biol Biochem 37:2180–2184

    Article  CAS  Google Scholar 

  • Ferreira LP, Lehman PS, Almeida AMR (1981) Moléstias e seu controle. In: Miyasaka S, Medina J (eds) A soja no Brasil. ITAL, Campinas, pp 603–639

    Google Scholar 

  • FRAC (2018) Fungicide Resistance Action Committee. FRAC fungicide list. Sorted by mode of action. http://www.phi-base.org/images/fracCodeList.pdf. Accessed 3 Oct 2019

  • Geraldine AM, Lopes FAC, Carvalho DDC, Barbosa ET, Rodrigues AR, Brandão RS, Ulhoa CJ, Lobo Junior M (2013) Cell wall-degrading enzymes and parasitism of sclerotia are key factors on field biocontrol of white mold by Trichoderma spp. Biol Control 67(3):308–316

    Article  CAS  Google Scholar 

  • Godoy G, Steadman JR, Dickman MB, Dam M (1990) Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Mol Plant Pathol 37:179–191

    Article  CAS  Google Scholar 

  • Grau CR, Hartman GL (2015) Sclerotinia stem rot. In: Hartman GL, Rupe JC, Sikora EF, Domier LL, Davis JA, Steffey KL (eds) Compendium of soybean diseases and pests. American Phytopathological Society, St. Paul, pp 59–62

    Google Scholar 

  • Guzmán-Guzmán P, Porras-Troncoso MD, Olmedo-Monfil V, Herrera-Estrella A (2019) Trichoderma species: versatile plant symbionts. Phytopathology 09:6–16

    Article  Google Scholar 

  • Haddad PE, Leite LG, Lucon CMM, Harakava R (2017) Selection of Trichoderma spp. strains for the control of Sclerotinia sclerotiorum in soybean. Pesq Agropecu Bras 52(12):1140–1148

    Article  Google Scholar 

  • Harman G (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194

    Article  CAS  PubMed  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  PubMed  Google Scholar 

  • Hartman GL, Kull L, Huang YH (1998) Occurrence of Sclerotinia sclerotiorum in soybean fields in East-Central Illinois and enumeration of inocula in soybean seed lots. Plant Dis 82:560–564

    Article  CAS  PubMed  Google Scholar 

  • Jackson MA, Kobori NN, Mascarin GM (2016) Trichoderma compositions and methods of use. Patent number WO2016044456. https://patentscope.wipo.int/search/en/detail.jsf;jsessionid=5CB3380A619515096A38627ACECE5D02.wapp1nA?docId=WO2016044456&tab=PCTDESCRIPTION

  • Jain A, Singh A, Singh S, Sarma B, Singh H (2014) Biocontrol agents-mediated suppression of oxalic acid induced cell death during Sclerotinia sclerotiorum and pea interaction. J Basic Microbiol 54:601–606

    Google Scholar 

  • Kobori NN, Mascarin GM, Jackson MA, Schisler DA (2015) Liquid culture production of microsclerotia and submerged conidia by Trichoderma harzianum active against damping-off disease caused by Rhizoctonia solani. Fungal Biol 119:179–190

    Article  CAS  PubMed  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–26

    Article  Google Scholar 

  • Lehner MS, Teixeira H, Paula Junior TJ, Vieira RF, Lima RC, Carneiro JES (2015) Adaptation and resistance to diseases in Brazil of putative sources of common bean resistance to white mold. Plant Dis 99:1098–1103

    Article  CAS  PubMed  Google Scholar 

  • Lenth RV (2018) emmeans: estimated marginal means, aka least-squares means [Computer software manual]. https://cran.r-project.org/package=emmeans (R package version 1.1.3)

  • Liu Y, Paul VH (2007) Studies on the germination of sclerotia of Sclerotinia sclerotiorum. J Plant Dis Prot 114(1):14–19

    Article  Google Scholar 

  • Milanesi P, Blume E, Antonioli Z, Muniz M, Santos R, dos Finger R, Durigon M (2013) Biocontrol of Fusarium spp. with Trichoderma spp. and promotion growth in soybean seedlings. Revista Ciênc Agr 36:347–356

    Google Scholar 

  • Mueller DS, Hartman GL, Pedersen WL (1999) Development of sclerotia and apothecia of Sclerotinia sclerotiorum from infected soybean seed and its control by fungicide seed treatment. Plant Dis 83:1113–1115

    Article  CAS  PubMed  Google Scholar 

  • Mueller DS, Wise K, Tylka G, Duault N (2015) Pesticides. In: Hartman GL, Rupe JC, Sikora EF, Domier LL, Davis JA, Steffey KL (eds) Compendium of soybean diseases and pests. American Phytopathological Society, St. Paul, pp 171–173

    Google Scholar 

  • Napoleao R, Nasser L, Lopes C, Filho A (2006) Neon-S, a new medium for detection of Sclerotinia sclerotiorum on seeds. Summa Phytopathol 32(2):180–182

    Article  CAS  Google Scholar 

  • Ousley M, Lynch J, Whipps JM (1994) Potential of Trichoderma spp. as consistent plant-growth stimulators. Biol Fertil Soils 17:85–90

    Article  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. ISBN 3-900051-07-0. http://www.r-project.org/

  • Resende ML, Oliveira JA, Guimarães RM, Von Pinho RG, Vieira AR (2004) Corn seed inoculation using Trichoderma harzianum as a growth promoter. Ciênc Agrotec 28(4):793–798

    Article  Google Scholar 

  • Rollins J (2003) The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant Microbe Interact 16:785–795

    Article  CAS  PubMed  Google Scholar 

  • Rollins J, Dickman MB (2001) pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Appl Environ Microbiol 67:75–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos A, Dhingra O (1982) Pathogenicity of Trichoderma spp. on the sclerotia of Sclerotinia sclerotiorum. Can J Bot 60:472–475

    Article  Google Scholar 

  • Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Sumida CH, Daniel JFS, Araujod APCS, Peitl DC, Abreu LM, Dekker RFH, Canteri MG (2018) Trichoderma asperelloides antagonism to nine Sclerotinia sclerotiorum strains and biological control of white mold disease in soybean plants. Biocontrol Sci Technol 28(2):142–156

    Article  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalbert E, Mara R, Barbetti MJ, Woo S, Lorito M (2008) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86

    Article  CAS  Google Scholar 

  • Vuong TD, Hoffman DD, Diers BW, Miller JF, Steadman JR, Hartman GL (2004) Evaluation of soybean, dry bean, and sunflower for resistance to Sclerotinia sclerotiorum. Crop Sci 44:777–783

    Google Scholar 

  • Warton D, Hui F (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Xiang Y, Herman T, Hartman GL (2014) Utilizing soybean milk to culture soybean pathogens. Adv Microbiol 4:126–132

    Article  CAS  Google Scholar 

  • Yadav S, Srivastava A, Singh D, Arora D (2012) Isolation of oxalic acid tolerating fungi and decipherization of its potential to control Sclerotinia sclerotiorum through oxalate oxidase like protein. World J Microbiol Biotechnol 28:3197–3206

    Article  CAS  PubMed  Google Scholar 

  • Yu D, Li C, Huang Y, Huang Z (2019) Joint action of Trichoderma hamatum and difenoconazole on growth of a phytopathogen Sclerotinia sclerotiorum under laboratory conditions. Pak J Zool 50(6):2249–2259

    Google Scholar 

Download references

Acknowledgements

The first author was the recipient of a doctorate scholarship (N. 250077/2013-2—SWE) and the second author received a post-doctoral scholarship (Project N. 245325/2012-3) both from CNPq (Brazilian National Council for Scientific and Technological Development). This work was partially sponsored by USDA Agricultural Research Service.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gabriel M. Mascarin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Jesus Marcado Blanco

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1287 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Macena, A.M.F., Kobori, N.N., Mascarin, G.M. et al. Antagonism of Trichoderma-based biofungicides against Brazilian and North American isolates of Sclerotinia sclerotiorum and growth promotion of soybean. BioControl 65, 235–246 (2020). https://doi.org/10.1007/s10526-019-09976-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-019-09976-8

Keywords

Navigation