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Antifungal activity against plant pathogens by compounds from Streptoverticillium morookaense

  • Mebeaselassie AndargieEmail author
  • Jianxiong Li
Original Article
  • 37 Downloads

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.

Keywords

Antifungal Biocontrol Ergosterol Streptoverticillium morookaense U. virens 

Notes

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.

Compliance with ethical standards

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.

Supplementary material

42161_2018_234_MOESM1_ESM.docx (60 kb)
ESM 1 (DOCX 60 kb)

References

  1. Agrios GN (2005) Plant pathology, 5th edn. Elsevier Acad Press, AmsterdamGoogle Scholar
  2. 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 85–92CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 69:211–217CrossRefGoogle Scholar
  5. 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 37:3332–3337Google Scholar
  6. 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 44:2081–2085CrossRefGoogle Scholar
  7. Bagga PS, Kaur S (2006) Evaluation of fungicides for controlling false smut (Ustilaginoidea virens) of rice. Indian Phytopathol 59:115–117Google Scholar
  8. Bauer AW, Kirby WM, Sherris JC, Turck M (1996) Antibiotic susceptibility testing by standardized single disc method. Am J Clin Pathol 44:493–496Google Scholar
  9. Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. Bressan W (2003) Biological control of maize seed pathogenic fungi by use of actinomycetes. BioControl 48:233–240CrossRefGoogle Scholar
  12. 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):152–164CrossRefGoogle Scholar
  13. 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 261:1852–1865CrossRefGoogle Scholar
  14. 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 71:231–239CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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):179–183CrossRefGoogle Scholar
  17. Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. PNAS 104:10282–10287CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 Google Scholar
  20. 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 67:3739–3745CrossRefGoogle Scholar
  21. 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 237–265CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 51:418–422CrossRefGoogle Scholar
  24. 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 Google Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 12:1–6Google Scholar
  27. 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 7:1869CrossRefGoogle Scholar
  28. 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
  29. 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 97:16–24CrossRefGoogle Scholar
  30. 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 33:120CrossRefGoogle Scholar
  31. Meij A, Worsley SF, Hutchings MI, Wezel GP (2017) Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev 41:392–416CrossRefGoogle Scholar
  32. 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 67:3418–3425CrossRefGoogle Scholar
  33. 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):301–302Google Scholar
  34. Montesinos E (2003) Development, registration and commercialization of microbial pesticides for plant protection. Int Microbiol 6:245–252CrossRefGoogle Scholar
  35. 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):2664–2669CrossRefGoogle Scholar
  36. Nega A (2014) Review on concepts in biological control of plant pathogens. J Biol Agric Healthc 4(27):33–54Google Scholar
  37. 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):280–292CrossRefGoogle Scholar
  38. 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 489:663–668CrossRefGoogle Scholar
  39. 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):28–31Google Scholar
  40. 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 58:1454–1462CrossRefGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. Rodriguez RJ, Low C, Bottema CD, Parks LW (1985) Multiple functions for sterols in Saccharomyces cerevisiae. Biochim Biophys Acta 837:336–343CrossRefGoogle Scholar
  43. Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29CrossRefGoogle Scholar
  44. 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):177–178Google Scholar
  45. Sharma RR, Singh D, Singh R (2009) Biological control of postharvest diseases on fruits and vegetables by microbial antagonists: a review. Biol Control 50:205–221CrossRefGoogle Scholar
  46. Singh S, Pal V, Panwar M (1992) False smut of rice—its impact on yield components. Crop Research Hisar 5:246–248Google Scholar
  47. Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect 5:535–544CrossRefGoogle Scholar
  48. 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 639–648Google Scholar
  49. 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 145:464–470CrossRefGoogle Scholar
  50. 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 72:301–304CrossRefGoogle Scholar
  51. Vining LC (1990) Function of secondary metabolites. Annu Rev Microbiol 44:395–427.  https://doi.org/10.1146/annurev.mi.44.100190.002143 CrossRefGoogle Scholar
  52. 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):54CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. Yang LM, Chen L, Xu J, Liu JC, Ding KJ (2012) Estimation of yield loss caused by rice false smut. J Anhui Agric Univ 39:474–477Google Scholar
  55. 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 55:129–132CrossRefGoogle Scholar
  56. 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 63:365–372CrossRefGoogle Scholar

Copyright information

© Società Italiana di Patologia Vegetale (S.I.Pa.V.) 2019

Authors and Affiliations

  1. 1.Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement, and Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  2. 2.Department of Crop SciencesGeorg-August-Universität GöttingenGöttingenGermany
  3. 3.College of Life ScienceYangtze UniversityJingzhouChina

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