Assessing the prospects of Streptomyces sp. RP1A-12 in managing groundnut stem rot disease caused by Sclerotium rolfsii Sacc

Journal of General Plant Pathology volume 82, pages96–104(2016)Cite this article

Abstract

Stem rot of groundnut caused by the soilborne pathogen Sclerotium rolfsii can cause significant yield losses. Biological control of stem rot using actinomycetes is a viable alternative to existing fungicidal management. Though actinomycetes are prolific antibiotic producers, reports pertaining to their use in groundnut disease management are limited. Here, actinomycetes were isolated from groundnut rhizospheric soils and screened for antagonism against S. rolfsii through a dual culture assay. Culture filtrates and crude extracts of the potential candidates were screened further for extracellular antifungal activity and characterized for biocontrol and plant-growth-promoting traits. A promising candidate was tested under greenhouse conditions as whole organism as well as crude extracts. Isolate RP1A-12 exhibited high antagonism against S. rolfsii in dual culture assay (69 % inhibition), culture filtrate assay (78–100 % inhibition at various concentrations) and crude extract assay (100 % inhibition with 1 % crude extracts). Moreover, germination of sclerotia of the test pathogen was inhibited with 1 % crude extracts. Strain RP1A-12 produced hydrogen cyanide, lipase, siderophores and indole acetic acid. Oxalic acid production by S. rolfsii was also inhibited by crude extracts of RP1A-12. In greenhouse studies, RP1A-12 reduced stem rot severity. Overall, our results suggest that isolate RP1A-12 has potential biocontrol capabilities against stem rot pathogen. Molecular characterization based on 16S rRNA gene sequencing of RP1A-12 identified it as a species of Streptomyces, closely related to S. flocculus.

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References

  1. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    Article  CAS  PubMed  Google Scholar 

  2. Aldesuquy HS, Mansour FA, Abo-Hamed SA (1998) Effect of the culture filtrates of Streptomyces on growth and productivity of wheat plants. Folia Microbiol 43:465–470

    Article  Google Scholar 

  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  4. Anjaiah V, Cornelis P, Koedam N (2003) Effect of genotype and root colonization in biological control of fusarium wilts in pigeonpea and chickpea by Pseudomonas aeruginosa PNA1. Can J Microbiol 49:85–91

    Article  CAS  PubMed  Google Scholar 

  5. Bhattacharya A, Chandra S, Barik S (2009) Lipase and protease producing microbes from the environment of sugar beet field. Ind J Agric Biochem 22:26–30

    CAS  Google Scholar 

  6. Bouizgarne B (2013) Bacteria for plant growth promotion and disease management. In: Maheshwari DK (ed) Bacteria in agrobiology: disease management. Springer, Heidelberg, pp 15–47

    Google Scholar 

  7. Bowen KL, Hagan AK, Weeks R (1992) Seven years of Sclerotium rolfsii in peanut fields: yield losses and means of minimization. Plant Dis 76:982–985

    Article  Google Scholar 

  8. Cessna SG, Sears VE, Dickman MB, Low PS (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 12:2191–2200

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  9. Chaiharn M, Chunhaleuchanon S, Lumyong S (2009) Screening siderophore producing bacteria as potential biological control agent for fungal rice pathogens in Thailand. World J Microbiol Biotechnol 25:1919–1928

    Article  Google Scholar 

  10. Crawford DL, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Appl Environ Microbiol 59:3899–3905

    PubMed Central  CAS  PubMed  Google Scholar 

  11. Dennis C, Webster J (1971) Antagonistic properties of species-groups of Trichoderma: III. Hyphal interaction. Trans Br Mycol Soc 57:363–369

    Article  Google Scholar 

  12. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394

    Article  CAS  PubMed  Google Scholar 

  13. Doumbou CL, Salove MKH, Crawford DL, Beaulieu C (2001) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82:85–102

    Article  Google Scholar 

  14. Duijff BJ, Meijer JW, Bakker PAHM, Schippers B (1993) Siderophore-mediated competition for iron and induced resistance in the suppression of fusarium wilt of carnation by fluorescent Pseudomonas spp. Neth J Plant Pathol 99:277–289

    Article  CAS  Google Scholar 

  15. El-Tarabily KA, Soliman MH, Nassar AH, Al-Hassani HA, Sivasithamparam K, McKenna F, Hardy GS (2000) Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes. Plant Pathol 49:573–583

    Article  Google Scholar 

  16. Endo A, Kakiki K, Misato T (1970) Mechanism of action of the antifungal agent polyoxin D. J Bacteriol 104:189–196

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Gawande SP, Borkar SG, Chimote VP (2013) Variation in growth and oxalic acid production by different crop isolates of Sclerotium rolfsii Sacc. J Mycopathol Res 51:95–100

    Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Gopalakrishnan S, Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, Vidya MS, Deepthi K, Rupela O (2011) Evaluation of actinomycete isolates obtained from herbal vermicompost for the biological control of Fusarium wilt of chickpea. Crop Prot 30:1070–1078

    Article  CAS  Google Scholar 

  20. Gopalakrishnan S, Srinivas V, Vidya, Rathore A (2013) Plant growth-promoting activities of Streptomyces spp. in sorghum and rice. SpringerPlus 2:574

    PubMed Central  Article  PubMed  Google Scholar 

  21. Gyaneshwar P, Naresh Kumar G, Parekh LJ (1998) Effect of buffering on the phosphate-solubilizing ability of microorganisms. World J Microbiol Biotechnol 14:669–673

    Article  CAS  Google Scholar 

  22. Hagan AK, Weeks JR, Bowen K (1991) Effects of application timing and method on control of southern stem rot of peanut with foliar-applied fungicides. Peanut Sci 18:47–50

    Article  Google Scholar 

  23. Hagan AK, Campbell HL, Bowen KL, Wells L, Goodman R (2010) Managing early leaf spot and stem rot with reduced fungicide inputs on disease-resistant peanut cultivars. Peanut Sci 37:129–136

    Article  Google Scholar 

  24. Hirano S, Nagao N (1988) An improved method for the preparation of colloidal chitin by using methanesulfonic acid. Agric Biol Chem 52:2111–2112

    Article  CAS  Google Scholar 

  25. Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160:778–788

    Article  CAS  PubMed  Google Scholar 

  26. Kortemaa H, Rita H, Haahtela K, Smolander A (1994) Root-colonization ability of antagonistic Streptomyces griseoviridis. Plant Soil 163:77–83

    Google Scholar 

  27. Le CN (2011) Diversity and biological control of Sclerotium rolfsii, causal agent of stem rot of groundnut. PhD thesis, Wageningen University, Wageningen

  28. Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1:142–146

    Article  CAS  Google Scholar 

  29. Macagnan D, Romeiro RS, Pomella AWV, deSouza JT (2008) Production of lytic enzymes and siderophores, and inhibition of germination of basidiospores of Moniliophthora (ex Crinipellis) perniciosa by phylloplane actinomycetes. Biol Control 47:309–314

    Article  CAS  Google Scholar 

  30. Mahadevan A, Sridhar R (1986) Methods in physiological plant pathology, 3rd edn. Sivakami, Madras, p 182

    Google Scholar 

  31. Mayee CD, Datar VV (1988) Diseases of groundnut in the tropics. Rev Trop Plant Pathol 5:85–118

    Google Scholar 

  32. Nene YL, Thapliyal PN (1993) Fungicides in plant disease control, 3rd edn. Oxford and IBH Publishing, New Delhi

    Google Scholar 

  33. Pande S, Rao JN (2000) Changing scenario of groundnut diseases in Andhra Pradesh, Karnataka and Tamil Nadu states of India. Int Arachis Newsl 20:42–44

    Google Scholar 

  34. Paramasivan M, Mohan S, Muthukrishnan N, Chandrasekaran A (2013) Degradation of oxalic acid (OA) producing Sclerotium rolfsii (Sacc.) by organic biocides. Arch Phytopath Plant Prot 46:357–363

    Article  CAS  Google Scholar 

  35. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    Article  CAS  PubMed  Google Scholar 

  36. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  37. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  38. Seong CN, Choi JH, Baik KS (2001) An improved selective isolation of rare actinomycetes from forest soil. J Microbiol 39:17–23

    Google Scholar 

  39. Shokes FM, Róźalski K, Gorbet DW, Brenneman TB, Berger DA (1996) Techniques for inoculation of peanut with Sclerotium rolfsii in the greenhouse and field. Peanut Sci 23:124–128

    Article  Google Scholar 

  40. Sterner O (2012) Isolation of microbial natural products. In: Sarker SD, Nahar L (eds) Natural products isolation. Methods in molecular biology, vol. 864. Springer Protocols, Heidelberg pp 393–413

  41. Stockwell VO, Duffy B (2012) Use of antibiotics in plant agriculture. Rev Sci Tech Off Int Epiz 31:199–210

    CAS  Google Scholar 

  42. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  43. Thompson JD, Gibsom TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  44. Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant–microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  45. Trejo-Estrada SR, Paszczynski A, Crawford DL (1998) Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. J Ind Microbiol Biotechnol 21:81–90

    Article  CAS  Google Scholar 

  46. Valois D, Fayad K, Barasubiye T, Garon M, Dery C, Brzezinski R, Beaulieu C (1996) Glucanolytic actinomycetes antagonistic to Phytophthora fragariae var. rubi, the causal agent of raspberry root rot. Appl Environ Microbiol 62:1630–1635

    PubMed Central  CAS  PubMed  Google Scholar 

  47. Vidhyasekaran P, Muthamilan M (1995) Development of formulations of Pseudomonas fluorescens for control of chickpea wilt. Plant Dis 79:782–786

    Article  Google Scholar 

  48. Voisard C, Keel C, Haas D, Défago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 8:351–358

    PubMed Central  CAS  PubMed  Google Scholar 

  49. Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 612:3119–3128

    Google Scholar 

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Acknowledgments

The authors are thankful to Biotechnology Industry Research Assistance Council (BIRAC), A Government of India Enterprise, for providing financial support under Biotechnology Industry Partnership Programme (BIPP) scheme (Proposal No. BT/BIPP0429/11/10). The authors are also thankful to Sri Biotech Laboratories India Pvt. Ltd, Hyderabad, India for their collaboration on this project.

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  1. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, 502324, India

    Simi Jacob, K. Vijay Krishna Kumar, Rajeev Varshney & Hari Kishan Sudini

  2. Jawaharlal Nehru Technological University, Kukatpally, Hyderabad, 500085, India

    Simi Jacob

  3. Department of Biotechnology, Sreenidhi Institute of Science and Technology, Hyderabad, 501301, Telangana, India

    Ramgopal Rao Sajjalaguddam

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  1. Simi Jacob
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Correspondence to Hari Kishan Sudini.

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Jacob, S., Sajjalaguddam, R.R., Kumar, K.V.K. et al. Assessing the prospects of Streptomyces sp. RP1A-12 in managing groundnut stem rot disease caused by Sclerotium rolfsii Sacc. J Gen Plant Pathol 82, 96–104 (2016). https://doi.org/10.1007/s10327-016-0644-0

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Keywords

  • Groundnut
  • Stem rot
  • Biocontrol
  • Streptomyces sp.
  • Antifungal metabolites