Skip to main content
Log in

Antifungal activity against plant pathogens by compounds from Streptoverticillium morookaense

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

Abstract

Biological control of pathogens by endophytes is a promising approach. The present study reports the significant impact of an antifungal compound that is isolated from Streptoverticillium morookaense as a potential biocontrol agent. This antifungal compound demonstrated a significant inhibitory activity against the three phytopathogenic fungi, Ustilaginoidea virens, Rhizoctonia solani and Bipolaris maydis and resulted in severe morphological distortions in their structure. Minimal inhibitory concentrations of the compound ranged from 50 to 150 μg/ml. In vitro evaluation of the compound showed strong control efficacy against U. virens, a causative agent of rice false smut fungus, on susceptible rice seedlings. In addition, it promoted plant growth with increased rate of seed germination and displayed no phytotoxicity. This compound also showed stability after its exposure to a temperature of 100 °C. The antifungal metabolite produced by this actinomycete may be developed as a safe and ideal bio-fungicide for the control of different fungal plant diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Agrios GN (2005) Plant pathology, 5th edn. Elsevier Acad Press, Amsterdam

    Google Scholar 

  • Alivizatos AS, Pantazius S (1992) Preliminary studies on biological control of potato common scab caused by Streptomyces sp. In: Tjamos ES (ed) Biological control of plant diseases. Plenum Press, New York, pp 85–92

    Chapter  Google Scholar 

  • Andresen M, Wulff EG, Mbega ER, Stokholm MS, Glazowska SE, Zida PE (2015) Seed treatment with an aqueous extract of Agave sisalana improves seed health and seedling growth of sorghum. Eur J Plant Pathol 141:119–132. https://doi.org/10.1007/s10658-014-0530-6

    Article  Google Scholar 

  • Aremu EA, Furumai T, Igarashi Y, Sato Y, Akamatsu H, Kodama M, Otani H (2003) Specific inhibition of spore germination of Alternaria brassicicola by fistupyrone from Streptomyces sp. TP−A0569. J Gen Plant Pathol 69:211–217

    Article  CAS  Google Scholar 

  • Arthington-Skaggs BA, Jradi H, Desai T, Morrison CJ (1999) Quantitation of ergosterol content: novel method for determination of fluconazole susceptibility of Candida albicans. J Clin Microbiol 37:3332–3337

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arthington-Skaggs BA, Warnock DW, Morrison CJ (2000) Quantitation of Candida albicans ergosterol content improves the correlation between in vitro antifungal susceptibility test results and in vivo outcome after fluconazole treatment in a murine model of invasive candidiasis. Antimicrob Agents Chemother 44:2081–2085

    Article  CAS  Google Scholar 

  • Bagga PS, Kaur S (2006) Evaluation of fungicides for controlling false smut (Ustilaginoidea virens) of rice. Indian Phytopathol 59:115–117

    Google Scholar 

  • Bauer AW, Kirby WM, Sherris JC, Turck M (1996) Antibiotic susceptibility testing by standardized single disc method. Am J Clin Pathol 44:493–496

    Google Scholar 

  • Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26

    Article  CAS  Google Scholar 

  • Bordoloi GN, Kumari B, Guha A, Thakur D, Bordoloi M, Roy MK (2002) Potential of a novel antibiotic, 2-methyl heptyl iso-nicotinate, as a biocontrol agent against fusarial wilt of crucifers. Pest Manag Sci 58:297–302. https://doi.org/10.1002/ps.457

    Article  CAS  PubMed  Google Scholar 

  • Bressan W (2003) Biological control of maize seed pathogenic fungi by use of actinomycetes. BioControl 48:233–240

    Article  Google Scholar 

  • Chung EJ, Hossain MT, Khan A, Kim KH, Jeon CO, Chung YR (2015) Bacillus oryzicola sp. nov., an endophytic bacterium isolated from the roots of rice with antimicrobial, plant growth promoting, and systemic resistance inducing activities in rice. Plant Pathol J 31(2):152–164

    Article  Google Scholar 

  • Coleman TW, Grulke NE, Daly M, Godinez C, Schilling SL, Riggan PJ, Seybold SJ (2011) Coast live oak, Quercus agrifolia, susceptibility and response to goldspotted oak borer, Agrilus auroguttatus, injury in southern California. For Ecol Mang 261:1852–1865

    Article  Google Scholar 

  • Díaz-Dellavalle P, Cabrera A, Alem D, Larrañaga P, Ferreira F, Dalla-Rizza M (2011) Antifungal activity of medicinal plant extracts against phytopathogenic fungus Alternaria spp. Chilean J Agric Res 71:231–239

    Article  Google Scholar 

  • El-Tarabily KA, Sivasithamparam K (2006) Non-streptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biol Biochem 38:1505–1520. https://doi.org/10.1016/j.soilbio.2005.12.017

    Article  CAS  Google Scholar 

  • Feng N, Ye W, Wu P, Huang Y, Xie H, Wei X (2007) Two new antifungal alkaloids produced by Streptoverticillium morookaense. J Antibiot 60(3):179–183

    Article  CAS  Google Scholar 

  • Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. PNAS 104:10282–10287

    Article  CAS  Google Scholar 

  • García PC, Rivero RM, Ruiz JM, Romero L (2003) The role of fungicides in the physiology of higher plants: implications for defense responses. Bot Rev 69:162–172. https://doi.org/10.1663/0006-8101

    Article  Google Scholar 

  • Gunji S, Arima K, Beppu T (1983) Screening of antifungal antibiotics according to activities inducing morphological abnormalities. Agric Biol Chem 47:2061–2069. https://doi.org/10.1271/bbb1961.47.2061

    Article  CAS  Google Scholar 

  • Hwang BK, Lim SW, Kim BS, Lee JY, Moon SS (2001) Isolation and in vivo and in vitro antifungal activity of phenylacetic acid and sodium phenylacetate from Streptomyces humidus. Appl Environ Microbiol 67:3739–3745

    Article  CAS  Google Scholar 

  • Jayaprakashvel M, Mathivanan N (2011) Management of plant diseases by microbial metabolites. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer-Verlag, Berlin, Heidelberg, pp 237–265

    Chapter  Google Scholar 

  • Kavitha A, Prabhakar P, Vijayalakshmi M, Venkateswarlu Y (2010) Purification and biological evaluation of the metabolites produced by Streptomyces sp. TK-VL_333. Res Microbiol 161:335–345. https://doi.org/10.1016/j.resmic.2010.03.011

    Article  CAS  PubMed  Google Scholar 

  • Koiso Y, Morisaki N, Yamashita Y, Mitsui Y, Shirai R, Hashimoto Y, Iwasaki S (1998) Isolation and structure of an antimitotic cyclic peptide, ustiloxin F: chemical interrelation with a homologous peptide, ustiloxin B. J Antibiot 51:418–422

    Article  CAS  Google Scholar 

  • Law JW, Ser HL, Khan TM, Chuah LH, Pusparajah P, Chan KG, Goh BH, Lee LH (2017) The potential of Streptomyces as biocontrol agents against the rice blast fungus, Magnaporthe oryzae (Pyricularia oryzae). Front Microbiol 8:3. https://doi.org/10.3389/fmicb.2017.00003

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Q, Jiang Y, Ning P, Zheng L, Huang J, Li G (2011) Suppression of Magnaporthe oryzae by culture filtrates of Streptomyces globisporus JK-1. Biol Control 58:139–148. https://doi.org/10.1016/j.biocontrol.2011.04.013

    Article  CAS  Google Scholar 

  • Loliam B, Morinaga T, Chaiyanan S (2012) Biocontrol of phytwophthora infestans, fungal pathogen of sedling damping off disease in economic plant nursery. Hindawi Publishing Corporation Psyche 12:1–6

  • Manhas K, Kaur T (2016) Biocontrol potential of Streptomyces hydrogenans strain DH16 toward Alternaria brassicicola to control damping off and black leaf spot of Raphanus sativus. Front Plant Sci 7:1869

    Article  Google Scholar 

  • Martinez JA (2012) Natural fungicides obtained from plants, fungicides for plant and animal diseases. In Dhanasekaran D (ed) ISBN: 978–953–307-804-5, InTech. https://doi.org/10.5772/26336

  • Mebeaselassie A, Luoye L, Aiqing F, Xiaoyuan Z, Jianxiong L (2015) Development of GFP-expressing Ustilaginoidea virens strain to study fungal invasion and colonization in rice spikelets. S Afr J Bot 97:16–24

    Article  Google Scholar 

  • Mebeaselassie A, Congyi Z, Yun Y, Jianxiong L (2017) Identification and evaluation of potential bio-control fungal endophytes against Ustilaginoidea virens on rice plants. World J Microbiol Biotechnol 33:120

    Article  Google Scholar 

  • Meij A, Worsley SF, Hutchings MI, Wezel GP (2017) Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev 41:392–416

    Article  Google Scholar 

  • Moënne-Loccoz Y, Tichy HV, O'Donnell A, Simon R, O'Gara F (2001) Impact of 2,4-diacetylphloroglycenol-producing biocontrol strain Pseudomonas fluorescens F113 on intraspecies diversity of resident culturable fluorescent pseudomonads associated with the roots of field-grown sugar beet seedlings. Appl Environ Microbiol 67:3418–3425

    Article  Google Scholar 

  • Mohiddin FA, Bhat FA, Gupta V, Gupta D, Kalha CS (2012) Integrated disease management of false smut of rice caused by Ustilaginoidea virens. Trends in Biosci 5(4):301–302

    Google Scholar 

  • Montesinos E (2003) Development, registration and commercialization of microbial pesticides for plant protection. Int Microbiol 6:245–252

    Article  CAS  Google Scholar 

  • Muniraju KM, Pramesh D, Mallesh SB, Mallikarjun K, Guruprasad GS (2017) Novel fungicides for the management of false smut disesases of rice caused by Ustilaginoidea virens. Int J Curr Microbiol App Sci 6(11):2664–2669

    Article  Google Scholar 

  • Nega A (2014) Review on concepts in biological control of plant pathogens. J Biol Agric Healthc 4(27):33–54

    Google Scholar 

  • Olaf T, Song C, Dickschat JS, Vos M, Garbeva P (2017) The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol 25(4):280–292

    Article  Google Scholar 

  • Ozaktan H, Bora T, Sukan S, Sargin S, Sukan FV (1999) Studies on determination on antagonistic potential and biopreparation of some bacteria against the fireblight pathogen. Acta Hortic 489:663–668

    Article  Google Scholar 

  • Pannu PPS, Thind TS, Goswami S (2010) Cultural studies on Ustilaginoidea virens, the incitant of false smut of rice (Oriza sativa). Indian J Agric Sci 85(7):28–31

    Google Scholar 

  • Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L (2009) Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, aspergillus and dermatophyte species. J Med Microbiol 58:1454–1462

    Article  Google Scholar 

  • Prapagdee B, Kuekulvong C, Mongkolsuk S (2008) Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. Int J Biol Sci 4:330–337. https://doi.org/10.7150/ijbs.4.330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez RJ, Low C, Bottema CD, Parks LW (1985) Multiple functions for sterols in Saccharomyces cerevisiae. Biochim Biophys Acta 837:336–343

    Article  CAS  Google Scholar 

  • Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29

    Article  CAS  Google Scholar 

  • Sharma RC, Gill SS, Randhawa HS (1994) Vitavax-an effective seed dresser for combined control ofstripe disease and smuts of Barley. Seed Res 22(2):177–178

  • Sharma RR, Singh D, Singh R (2009) Biological control of postharvest diseases on fruits and vegetables by microbial antagonists: a review. Biol Control 50:205–221

    Article  Google Scholar 

  • Singh S, Pal V, Panwar M (1992) False smut of rice—its impact on yield components. Crop Research Hisar 5:246–248

    Google Scholar 

  • Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect 5:535–544

    Article  CAS  Google Scholar 

  • Tank N, Rajendran N, Patel B, Saraf M (2012) Evaluation and biochemical characterization of a distinctive pyoverdin from a Pseudomonas isolated from chickpea rhizosphere. Braz J Microbiol 639–648

  • Tian J, Ban XQ, Zeng H, He JS, Huang B, Wang YW (2011) Chemical composition and antifungal activity of essential oil from Cicuta virosa L. var latisecta Celak. Int J Food Microbiol 145:464–470

    Article  CAS  Google Scholar 

  • Tsuda M, Sasahara M, Ohara T, Kato S (2006) Optimal application timing of simeconazole granules for control of rice kernel smut and false smut. J Gene Plant Pathol 72:301–304

    Article  CAS  Google Scholar 

  • Vining LC (1990) Function of secondary metabolites. Annu Rev Microbiol 44:395–427. https://doi.org/10.1146/annurev.mi.44.100190.002143

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang J, Lai D, Wang W, Dai J, Zhou L, Liu Y (2017) Ustiloxin G, a new cyclopeptide mycotoxin from rice false smut balls. Toxins 9(2):54

    Article  Google Scholar 

  • Wilson D (1995) Endophytes—the evolution of the term, a clarification of its use and definition. Oikos 73:274–276. https://doi.org/10.2307/3545919

    Article  Google Scholar 

  • Yang LM, Chen L, Xu J, Liu JC, Ding KJ (2012) Estimation of yield loss caused by rice false smut. J Anhui Agric Univ 39:474–477

    Google Scholar 

  • Yenjit P, Issarakraisila M, Intana W, Chantrapromma K (2010) Fungicidal activity of compounds extracted from the pericarp of Areca catechu against Colletotrichum gloesporioides in vitro and in mango fruit. Postharvest Biol Technol 55:129–132

    Article  CAS  Google Scholar 

  • Zhou YL, Xie XW, Zhang F, Wang S, Liu XZ, Zhu LH, Xu JL, Gao YM, Li ZK (2014) Detection of quantitative resistance loci associated with resistance to rice false smut (Ustilaginoidea virens) using introgression lines. Plant Pathol 63:365–372

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Sciences Foundation of China (30970627) and the fund for the Important Direction Research on Knowledge Innovation Project (KSCX2-EW-N-06) from CAS awarded to J.X. Li. M. Andargie was a recipient of the ‘Visiting Fellowship for Researchers from Developing Countries’ Award (2013FFSA0005) from Chinese Academy of Sciences. We would like to thank Prof Xiaoyi Wei for providing the metabolites that were extracted from S. morookaense.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mebeaselassie Andargie.

Ethics declarations

Conflict of interest

There is no conflict of interest in this study.

Ethical approval

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

Additional information

Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 60 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andargie, M., Li, J. Antifungal activity against plant pathogens by compounds from Streptoverticillium morookaense. J Plant Pathol 101, 547–558 (2019). https://doi.org/10.1007/s42161-018-00234-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42161-018-00234-x

Keywords