Skip to main content
SpringerLink
Log in

Mechanism of in vitro antagonism of phytopathogenic Scelrotium rolfsii by actinomycetes

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

Abstract

Sclerotium rolfsii (Sr), a soil-borne fungal pathogen, causes disease in a wide range of crops. Recently, we identified five actinomycetes (Streptomyces globisporus subsp. globisporus, S. globisporus, S. flavotricini, S. pactum, and S. senoensis) showing significant inhibitory effects on plant pathogens. In this study, the effects of the five actinomycetes for the biocontrol of Sr were investigated using the plate culture method and microscopy examination. Two actinomycetes with higher inhibitory effect were subsequently examined for the inhibition of sclerotial germination of Sr in unsterile soil in vitro. The cell-free cultures of five actinomycetes mediated significant inhibition of hyphal growth and sclerotial formation and germination of Sr. All actinomycete strains exhibited the ability to produce extracellular cell wall degrading enzymes in the culture conditions. The crude enzyme suspensions of S. flavotricini and S. pactum hydrolyzed the cell wall of Sr. At a dose of 1 g per kilogram soil, the solid formulations of S. flavotricini and S. senoensis prevented germination of 24% and 68% of sclerotia, respectively. Our results provide evidence of effective strains for the biocontrol of Sr, in addition to a further understanding of the underlying mechanism.

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

  • Abd-Allah, E. F. (2005). Effect of a Bacillus subtilis isolate on southern blight (Sclerotium rolfsii) and lipid composition of peanut seeds. Phytoparasitica, 33(5), 460–466.

    Article  Google Scholar 

  • Al-Askar, A. A., Baka, Z. A., Rashad, Y. M., Ghoneem, K. M., Abdulkhair, W. M., Hafez, E. E., et al. (2015). Evaluation of Streptomyces griseorubens E44G for the biocontrol of Fusarium oxysporum f. Sp. lycopersici: Ultrastructural and cytochemical investigations. Annals of Microbiology, 65(4), 1815–1824.

    Article  CAS  Google Scholar 

  • Baltz, R. H. (2016). Genetic manipulation of secondary metabolite biosynthesis for improved production in Streptomyces and other actinomycetes. Journal of Industrial Microbiology & Biotechnology, 43(2–3), 343–370.

    Article  CAS  Google Scholar 

  • Benhamou, N., & Chet, I. (1996). Parasitism of sclerotia of Sclerotium rolfsii by Trichoderma harzianum: Ultrastructural and cytochemical aspects of the interaction. Phytopathology, 86(4), 405–416.

    Article  Google Scholar 

  • Boukaew, S., Chuenchit, S., & Petcharat, V. (2011). Evaluation of Streptomyces spp. for biological control of Sclerotium root and stem rot and Ralstonia wilt of chilli pepper. BioControl, 56(3), 365–374.

    Article  Google Scholar 

  • Bowen, K. L., Hagan, A. K., & Weeks, R. (1992). Seven years of Sclerotium rolfsii in peanut fields: Yield losses and means of minimization. Plant Disease, 76(10), 982–985.

    Article  Google Scholar 

  • Carrieri, R., Cozzolino, E., Tarantino, P., Cerrato, D., & Lahoz, E. (2015). First report of southern blight on candyleaf (Stevia rebaudiana) caused by Sclerotium rolfsii in Italy. Plant Disease, 100(1), 220–221.

    Article  Google Scholar 

  • Derbalah, A. S., Dewir, Y. H., & El-Sayed, E. N. B. (2012). Antifungal activity of some plant extracts against sugar beet damping-off caused by Sclerotium rolfsii. Annals of Microbiology, 62(3), 1021–1029.

    Article  Google Scholar 

  • Duan, J. L., Xue, Q. H., Shu, Z. M., Wang, D. S., & He, F. (2015). Effects of combined application of actinomycetes Act12 bio-control agents and potassium humate on growth and microbial flora in rooting zone of Salvia miltiorrhiza Bge. Acta Ecologica Sinica, 35(6), 1807–1819.

    Google Scholar 

  • Elad, Y. (1995). Mycoparasitism. In K. Kohmoto, U. S. Singh, & R. P. Singh (Eds.), Pathogenesis and host specificity in plant diseases: Histopathological, biochemical, genetic and molecular bases. Vol II: Eukaryotes (pp. 285–307). Oxford: Pergamon Press.

    Google Scholar 

  • El-Tarabily, K. A., & Sivasithamparam, K. (2006). Non-streptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biology & Biochemistry, 38(7), 1505–1520.

    Article  CAS  Google Scholar 

  • Errakhi, R., Bouteau, F., Lebrihi, A., & Barakate, M. (2007). Evidences of biological control capacities of Streptomyces spp. against Sclerotium rolfsii responsible for damping-off disease in sugar beet (Beta vulgaris L.). World Journal of Microbiology and Biotechnology, 23(11), 1503–1509.

    Article  CAS  Google Scholar 

  • Errakhi, R., Lebrihi, A., & Barakate, M. (2009). In vitro and in vivo antagonism of actinomycetes isolated from Moroccan rhizospherical soils against Sclerotium rolfsii: A causal agent of root rot on sugar beet (Beta vulgaris L.). Journal of Applied Microbiology, 107(2), 672–681.

    Article  CAS  PubMed  Google Scholar 

  • Gamliel, A., & Katan, J. (1993). Suppression of major and minor pathogens by fluorescent pseudomonads in solarized and nonsolarized soils. Phytopathology, 83(1), 68–75.

    Google Scholar 

  • Gao, X. Y. (2010). Overview of southern blight in Chinese medicinal plants. Plant Diseases and Pests, 1(1), 28–34.

    CAS  Google Scholar 

  • Ghose, T. (1987). Measurement of cellulase activities. Pure and Applied Chemistry, 59(2), 257–268.

    Article  CAS  Google Scholar 

  • Goudjal, Y., Toumatia, O., Yekkour, A., Sabaou, N., Mathieu, F., & Zitouni, A. (2014). Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiological Research, 169(1), 59–65.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, R., Saxena, R. K., Chaturvedi, P., & Virdi, J. S. (1995). Chitinase production by Streptomyces viridificans: Its potential in fungal cell wall lysis. Journal of Applied Bacteriology, 78(4), 378–383.

    Article  CAS  PubMed  Google Scholar 

  • Haran, S., Schickler, H., & Chet, I. (1996). Molecular mechanisms of lytic enzymes involved in the biocontrol activity of Trichoderma harzianum. Microbiology, 142(9), 2321–2331.

    Article  CAS  Google Scholar 

  • Hata, E. M., Sijam, K., Ahmad, Z. A. M., Yusof, M. T., & Azman, N. A. (2015). In vitro antimicrobial assay of actinomycetes in rice against Xanthomonas oryzae pv. oryzicola and as potential plant growth promoter. Brazilian Archives of Biology and Technology, 58(6), 821–832.

    Article  CAS  Google Scholar 

  • He, F., Zhang, Z., Cui, M., & Xue, Q. H. (2015). Effect of biocontrol actinomycetes agents on microflora in the root-zone of Amorphophallus konjac K. Koch ex N.E.Br. Chinese Journal of Applied & Environmental Biology, 21(2), 221–227.

    Google Scholar 

  • Jacob, S., Sajjalaguddam, R. R., Kumar, K. V. K., Varshney, R., & Sudini, H. K. (2016). Assessing the prospects of Streptomyces sp. RP1A-12 in managing groundnut stem rot disease caused by Sclerotium rolfsii Sacc. Journal of General Plant Pathology, 82(2), 96–104.

    Article  CAS  Google Scholar 

  • Jogi, A., Kerry, J. W., Brenneman, T. B., Leebens-Mack, J. H., & Gold, S. E. (2016). Identification of genes differentially expressed during early interactions between the stem rot fungus (Sclerotium rolfsii) and peanut (Arachis hypogaea) cultivars with increasing disease resistance levels. Microbiological Research, 184(3), 1–12.

    Article  CAS  PubMed  Google Scholar 

  • John, N. S., Anjanadevi, I., Nath, V. S., Sankar, S. A., Jeeva, M. L., John, K. S., et al. (2015). Characterization of Trichoderma isolates against Sclerotium rolfsii, the collar rot pathogen of Amorphophallus – A polyphasic approach. Biological Control, 90(11), 164–172.

    Article  Google Scholar 

  • Koike, S. T. (2014). First report of southern blight of swiss chard (Beta vulgaris subsp. cicla) caused by Sclerotium rolfsii in California. Plant Disease, 98(6), 849–849.

    Article  Google Scholar 

  • Kotasthane, A., Agrawal, T., Kushwah, R., & Rahatkar, O. V. (2015). In-vitro antagonism of Trichoderma spp. against Sclerotium rolfsii and Rhizoctonia solani and their response towards growth of cucumber, bottle gourd and bitter gourd. European Journal of Plant Pathology, 141(3), 523–543.

    Article  CAS  Google Scholar 

  • Leoni, C., Braak, C. J. F. T., Gilsanz, J. C., Dogliotti, S., Rossing, W. A. H., & Bruggen, A. H. C. V. (2014). Sclerotium rolfsii dynamics in soil as affected by crop sequences. Applied Soil Ecology, 75(5), 95–105.

    Article  Google Scholar 

  • Li, Q., Ning, P., Zheng, L., Huang, J., Li, G., & Hsiang, T. (2012). Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biological Control, 61(2), 113–120.

    Article  CAS  Google Scholar 

  • Mahadevakumar, S., Yadav, V., Tejaswini, G. S., & Janardhana, G. R. (2016). Morphological and molecular characterization of Sclerotium rolfsii associated with fruit rot of Cucurbita maxima. European Journal of Plant Pathology, 145(1), 215–219.

    Article  CAS  Google Scholar 

  • Manjula, K., Kishore, G. K., Girish, A. G., & Singh, S. D. (2004). Combined application of Pseudomonas fluorescens and Trichoderma viride has an improved biocontrol activity against stem rot in groundnut. Plant Pathology Journal, 20(1), 75–80.

    Article  Google Scholar 

  • Muthukumar, A., & Venkatesh, A. (2014). Biological inductions of systemic resistance to collar rot of peppermint caused by Sclerotium rolfsii. Acta Physiologiae Plantarum, 36(6), 1421–1431.

    Article  CAS  Google Scholar 

  • Noronha, E. F., Kipnis, A., Junqueira-Kipnis, A. P., & Ulhoa, C. J. (2000). Regulation of 36-kDa β-1,3-glucanase synthesis in Trichoderma harzianum. FEMS Microbiology Letters, 188(1), 19–22.

    CAS  PubMed  Google Scholar 

  • Punja, Z. K. (1985). The biology, ecology, and control of Sclerotium rolfsii. Annual Review of Phytopathology, 23(1), 97–127.

    Article  CAS  Google Scholar 

  • Ristaino, J. B., Perry, K. B., & Lumsden, R. D. (1991). Effect of solarization and Gliocladium virens on sclerotia of Sclerotium rolfsii, soil microbiota, and the incidence of southern blight of tomato. Phytopathology, 81(10), 1117–1124.

    Article  Google Scholar 

  • Sennoi, R., Singkham, N., Jogloy, S., Boonlue, S., Saksirirat, W., Kesmala, T., & Patanothai, A. (2013). Biological control of southern stem rot caused by Sclerotium rolfsii using Trichoderma harzianum and arbuscular mycorrhizal fungi on Jerusalem artichoke (Helianthus tuberosus L.). Crop Protection, 54(12), 148–153.

    Article  Google Scholar 

  • Shanmugaiah, V., Mathivanan, N., Balasubramanian, N., & Manoharan, P. T. (2008). Optimization of cultural conditions for production of chitinase by Bacillus laterosporous MML2270 isolated from rice rhizosphere soil. African Journal of Biotechnology, 7(15), 2562–2568.

    CAS  Google Scholar 

  • Shen, G. H., Xue, Q. H., Chen, Q., Wang, L. N., Zhao, J., & Xue, L. (2012). Effects of combined application of potassium silicate and Streptomyces patum bio-control agents on growth, yield and quality of strawberry under continuous cropping in greenhouse. Chinese Journal of Eco-Agriculture, 20(3), 315–321.

    Article  CAS  Google Scholar 

  • Wei, X. L., Chen, J., He, F., Gu, M. Y., Wang, D. S., Xue, L., Duan, J. L., & Xu, W. L. (2013). Colonization and effects of antagonistic Streptomyces on leaf photosynthetic characteristics and growth of cotton seedlings. Journal of Northwest A&F University (Nat. Sci. Ed.), 41(9), 78–84 90.

    Google Scholar 

  • Wu, H., Li, J., Dong, D., Liu, T., Zhang, T., Zhang, D., & Liu, W. (2015). Heterologous coexpression of Vitreoscilla hemoglobin and Bacillus megaterium glucanase in Streptomyces lydicus A02 enhanced its production of antifungal metabolites. Enzyme and Microbial Technology, 81(12), 80–87.

    Article  CAS  PubMed  Google Scholar 

  • Xu, B., Chen, W., Wu, Z. M., Long, Y., & Li, K. T. (2015). A novel and effective Streptomyces sp. N2 against various phytopathogenic fungi. Applied Biochemistry and Biotechnology, 177(6), 1338–1347.

    Article  CAS  PubMed  Google Scholar 

  • You, J., Liu, H., & Huang, B. (2015). First report of southern blight caused by Sclerotium rolfsii on Macleaya cordata in China. Plant Disease, 100(2), 530–530.

    Article  Google Scholar 

  • Zhao, J., Xue, Q. H., & Tang, M. (2009). Screening of antagonistic actinomycetes against 'Jiashi' Cucumis melo L. damping-off. Journal of Northwest A&F University (Nat. Sci. Ed.), 37(5), 144–154.

    Google Scholar 

  • Zhao, J., Xue, Q. H., Wang, L. N., Duan, C. M., Xue, L., & Ning, M. (2011). Antagonistic effect of multifunctional actinomycete strain Act12 on soil-borne pathogenic fungi and its identification. Chinese Journal of Eco-Agriculture, 19(2), 394–398.

    Article  Google Scholar 

  • Zhao, J., Xue, Q. H., Shen, G. H., Xue, L., & Wang, D. S. (2012). Evaluation of Streptomyces spp. for biocontrol of gummy stem blight (Didymella bryoniae) and growth promotion of Cucumis melo L. Biocontrol Science & Technology, 22(1), 23–37.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Sci-Tech Support Plan (2012BAD14B11) and Shaanxi Science & Technology Co-ordination & Innovation Project (2016KTZDNY03-03-02). We thank Dr. Wentao Hu for providing a light microscope (Motic B5 Professional Series) in this study and Dr. Chaofeng Lin for improving the English in the manuscript.

Author information

Authors and Affiliations

  1. College of Natural Resources and Environment, Northwest A&F University, Yangling, 712100, China

    Yulong Li, Hangxian Lai & Quanhong Xue

  2. College of Forestry, Northwest A&F University, Yangling, 712100, China

    Fei He

Authors
  1. Yulong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hangxian Lai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Quanhong Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hangxian Lai or Quanhong Xue.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., He, F., Lai, H. et al. Mechanism of in vitro antagonism of phytopathogenic Scelrotium rolfsii by actinomycetes. Eur J Plant Pathol 149, 299–311 (2017). https://doi.org/10.1007/s10658-017-1177-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-017-1177-x

Keywords

Search

Navigation