Skip to main content
SpringerLink
Log in

The peculiar physiological responses of Rhizoctonia solani under the antagonistic interaction coupled by a novel antifungalmycin N2 from Streptomyces sp. N2

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

A novel antifungalmycin N2 (3-methyl-3,5-amino-4-vinyl-2-pyrone, C6H7O2N) was previously discovered from Streptomyces sp. N2, which exerted a broad-spectrum antagonistic activity against phytopathogenic fungi. To provide comprehensive insights into the antagonistic mechanisms and biocontrol efficacy of antifungalmycin N2, the present work investigated the physiological responses of Rhizoctonia solani under interaction with antifungalmycin N2. First, the mycelial growth of R. solani was significantly inhibited by antifungalmycin N2 during liquid shake-flask culture. Morphological observations showed that the morphogenesis of R. solani was influenced by antifungalmycin N2, in which the hyphae became severely shriveled and flattened, irregularly folded and branched. Additionally, an obvious accumulation of reactive oxygen species (ROS) was detected in R. solani hyphae, indicating oxidative stress induced by antifungalmycin N2. Further results showed that chitinase activity and its hydrolytic N-acetylglucosamine were significantly accelerated by antifungalmycin N2, demonstrating the cell wall of R. solani was damaged. Interestingly, the enzymatic antioxidant activities of R. solani were significantly induced in response to a relatively low concentration of antifungalmycin N2 (1.44–5.77 µg/mL). However, all antioxidant enzymes became highly inactive when the antifungalmycin N2 was increased to 11.53 µg/mL, suggesting that the enzymatic antioxidant system in R. solani was probably collapsed by the oxidative stress beyond its acceptance scope. In conclusion, antifungalmycin N2 exerted its antagonistic activity by inducing both cell wall degradation and oxidative stress in R. solani, thus leading to fungal morphogenesis and autolysis. Meanwhile, R. solani could induce and activate its antioxidant enzymes as a defence response to the oxidative stress caused by antifungalmycin N2.

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

  • Aguirre J, Rios-Momberg M, Hewitt D, Hansberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13:111–118

    Article  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Bio 55:373–399

    Article  CAS  Google Scholar 

  • Basu A, Chowdhury S, Ray Chaudhuri T, Kindu S (2016) Differential behaviour of sheath blight pathogen Rhizoctonia solani in tolerant and susceptible rice varieties before and during infection. Plant Pathol 8:1333–1346

    Article  CAS  Google Scholar 

  • Belozerskaya TA, Gessler NN (2007) Reactive oxygen species and the strategy of antioxidant defense in fungi: a review. Appl Biochem Microbiol 43:506–515

    Article  CAS  Google Scholar 

  • Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. Bioessays 28:799–808

    Article  PubMed  Google Scholar 

  • Chen YF, Zhou DB, Qi DF, Gao ZF, Xie JH, Luo YP (2017) Growth promotion and disease suppression ability of a Streptomyces sp. CB-75 from banana rhizosphere soil. Front Microbiol 8:2704

    Article  PubMed  Google Scholar 

  • Crowe JD, Olsson S (2001) Induction of laccase activity in Rhizoctonia solani by antagonistic Pseudomonas fluorescens strains and a range of chemical treatments. Appl Environ Microbiol 67:2088–2094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duffy B, Schouten A, Raaijmakers JM (2003) Pathogen self-defense: mechanisms to counteract microbial antagonism. Annu Rev Phytopathol 41:501–538

    Article  CAS  PubMed  Google Scholar 

  • Feng SJ, Shu CW, Wang CJZ, Jiang SF, Zhou EX (2017) Survival of Rhizoctonia solani AG-1 IA, the causal agent of rice sheath blight, under different environmental conditions. J Phytopathol 165:44–52

    Article  CAS  Google Scholar 

  • Fuentefria AM, Pippi B, Dalla Lana DF, De Andrade SF (2017) Antifungals discovery: an insight into new strategies to combat antifungal resistance. Lett Appl Microbiol 66:2–13

    Article  CAS  PubMed  Google Scholar 

  • Ghosh PG, Roy A, Hess D, Ghosh A, Das S (2015) Deciphering the mode of action of a mutant Allium sativum Leaf Agglutinin (mASAL), a potent antifungal protein on Rhizoctonia solani. BMC Microbiol 15:237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gkarmiri K, Finlay RD, Alstörm S, Thomas E, Cubeta MA, Högberg N (2015) Transcriptomic changes in the plant pathogenic fungus Rhizoctonia solani AG-3 in response to the antagonistic bacteria Serratia proteamaculans and Serratia plymuthica. BMC Genom 16:630

    Article  CAS  Google Scholar 

  • Gohel V, Singh A, Vimal M, Ashwini P, Chatpar HS (2006) Bioprospecting and antifungal potential of chitynolitic microorganisms. Afr J Biotechnol 5:54–72

    Google Scholar 

  • Hahn M (2014) The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J Chem Bio 7:133–141

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heller J, Tudzynski P (2011) Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 49:369–390

    Article  CAS  PubMed  Google Scholar 

  • Hoster F, Schmitz JE, Daniel R (2005) Enrichment of chitinolytic microorganisms: isolation and characterization of a chitinase exhibiting antifungal activity against phytopathogenic fungi from a novel Streptomyces strain. Appl Microbiol Biotechnol 66:434–442

    Article  CAS  PubMed  Google Scholar 

  • Labuschagne CF, Brenkman AB (2013) Current methods in quantifying ROS and oxidative damage in Caenorhabditis elegans and other model organism of aging. Ageing Res Rev 12:918–930

    Article  CAS  PubMed  Google Scholar 

  • Lehtonen MJ, Wilson PS, Ahvenniemi P, Valkonen JPT (2009) Formation of canker lesions on stems and black scurf on tubers in experimentally inoculated potato plants by isolates of AG2-1, AG3 and AG5 of Rhizoctonia solani: a pilot study and literature review. Agric Food Sci 18:223–233

    Article  Google Scholar 

  • Lupetti A, Danesi R, Campa M, Tacca MD, Kelly S (2002) Molecular basis of resistance to azole antifungals. Trends Mol Med 8:76–81

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Phys C 153:175–190

    Google Scholar 

  • Mazzola M, Freilich S (2016) Prospects for biological soil-borne disease control: application of indigenous versus synthetic microbiomes. Phytopathology 107:256–263

    Article  Google Scholar 

  • McSpadden Gardener BB, Driks A (2004) Overview of the nature and application of biocontrol microbes: Bacillus spp.. Phytopathology 94:1244

    Article  PubMed  Google Scholar 

  • Narayanasamy P (2013) Mechanisms of action of fungal biological control agents. In: Biological management of diseases of crops. progress in biological control, vol 14. Springer, Amsterdam, pp 99–200

    Chapter  Google Scholar 

  • Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361

    Article  CAS  Google Scholar 

  • Sahai AS, Manocha MS (1993) Chitinases of fungi and plants: their involvement in a morphogenesis and host/parasite interaction. FEMS Microbiol Rev 11:317–338

    Article  CAS  Google Scholar 

  • Tahvonen RT (2010) Microbial control of plant diseases with Streptomyces spp. 1. Eppo Bull 18:55–59

    Article  Google Scholar 

  • Tiwari IM, Jesuraj A, Kamboj R, Devanna BN, Botella JR, Sharma TR (2017) Host delivered RNAi, an efficient approach to increase rice resistance to sheath blight pathogen (Rhizoctonia solani). Sci Rep 7:7521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ubhayasekera W, Karlsson M (2012) Bacterial and fungal chitinase ChiJ orthologs evolve under different selective constraints following horizontal transfer. BMC Res Notes 5:581

    Article  PubMed  PubMed Central  Google Scholar 

  • Wahleithner JA, Xu F, Brown KM, Brown SH, Golightly EJ, Halkier T, Kauppinen S, Pederson A, Schneider P (1996) The identification and characterization of four laccases from the plant-pathogenic fungus Rhizoctonia solani. Curr Genet 29:395–403

    Article  CAS  PubMed  Google Scholar 

  • Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256

    Article  PubMed  Google Scholar 

  • Wu ZM, Yang Y, Li KT (2019) Antagonistic activity of a novel antifungalmycin N2 from Streptomyces sp. N2 and its biocontrol efficacy against Rhizoctonia solani. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fnz018

    Article  PubMed  Google Scholar 

  • Xu B, Chen W, Wu ZM, Long Y, Li KT (2015) A novel and effective Streptomyces sp. N2 against various phytopathogenic Fungi. Appl Biochem Biotechnol 177:1338–1347

    Article  CAS  PubMed  Google Scholar 

  • Yellareddygari SKR, Reddy MS, Kloepper JW, Lawrence KS, Fadamiro H (2014) Rice sheath blight: a review of disease and pathogen management approaches. J Plant Pathol Microbiol 5:4

    Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant no. 31760546), and the Training Program for Young Scientists of Jiangxi Provincial Department of Science and Technology (20142BCB23025).

Author information

Authors and Affiliations

  1. Jiangxi Engineering Laboratory for the Development and Utilization of Agricultural Microbial Resources, Jiangxi Agricultural University, Nanchang, 330045, China

    Yong Yang, Zhi-ming Wu & Kun-tai Li

Authors
  1. Yong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhi-ming Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kun-tai Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kun-tai Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Erko Stackebrandt.

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

Yang, Y., Wu, Zm. & Li, Kt. The peculiar physiological responses of Rhizoctonia solani under the antagonistic interaction coupled by a novel antifungalmycin N2 from Streptomyces sp. N2. Arch Microbiol 201, 787–794 (2019). https://doi.org/10.1007/s00203-019-01645-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-019-01645-9

Keywords

Search

Navigation