Skip to main content
SpringerLink
Log in

Characterization of Streptomyces spp. isolated from the rhizosphere of oil palm and evaluation of their ability to suppress basal stem rot disease in oil palm seedlings when applied as powder formulations in a glasshouse trial

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Ganoderma boninense, the main causal agent of oil palm (Elaeis guineensis) basal stem rot (BSR), severely reduces oil palm yields around the world. To reduce reliance on fungicide applications to control BSR, we are investigating the efficacy of alternative control methods, such as the application of biological control agents. In this study, we used four Streptomyces-like actinomycetes (isolates AGA43, AGA48, AGA347 and AGA506) that had been isolated from the oil palm rhizosphere and screened for antagonism towards G. boninense in a previous study. The aim of this study was to characterize these four isolates and then to assess their ability to suppress BSR in oil palm seedlings when applied individually to the soil in a vermiculite powder formulation. Analysis of partial 16S rRNA gene sequences (512 bp) revealed that the isolates exhibited a very high level of sequence similarity (> 98%) with GenBank reference sequences. Isolates AGA347 and AGA506 showed 99% similarity with Streptomyces hygroscopicus subsp. hygroscopicus and Streptomyces ahygroscopicus, respectively. Isolates AGA43 and AGA48 also belonged to the Streptomyces genus. The most effective formulation, AGA347, reduced BSR in seedlings by 73.1%. Formulations using the known antifungal producer Streptomyces noursei, AGA043, AGA048 or AGA506 reduced BSR by 47.4, 30.1, 54.8 and 44.1%, respectively. This glasshouse trial indicates that these Streptomyces spp. show promise as potential biological control agents against Ganoderma in oil palm. Further investigations are needed to determine the mechanism of antagonism and to increase the shelf life of Streptomyces formulations.

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
Fig. 5

Similar content being viewed by others

References

  • Alimuddin A, Widada J, Asmara W, Mustofa M (2011) Antifungal production of a strain of Actinomycetes spp. isolated from the rhizosphere of cajuput plant: selection and detection of exhibiting activity against tested fungi. Indones J Biotechnol 16(1):1–10

    Google Scholar 

  • Anderson AS, Wellington EM (2001) The taxonomy of Streptomyces and related genera. Int J Syst Evol Microbiol 51(3):797–814

    Article  CAS  Google Scholar 

  • Anitha A, Rabeeth M (2009) Control of Fusarium wilt of tomato by bioformulation of Streptomyces griseus in greenhouse condition. Afr J Basic Appl Sci 1:9–14

    Google Scholar 

  • Arif MA, Roslan A, Idris AS, Ramle M (2011) Economics of oil palm pests and Ganoderma disease and yield loses. In: Proceedings of the Third MPOB-IOPRI International Seminar: Integrated Oil Palm Pests and Disease Management, Kuala Lumpur, Malaysia. MPOB Publishing, pp 83–98

  • Awad MH, El-Shahed KYI, El-Nakkadi AEM (2009) Isolation, screening and identification of newly isolated soil Streptomyces (Streptomyces sp. NRC-35) for β-lactamase inhibitor production. World Appl Sci J 7(5):637–646

    Google Scholar 

  • Azizah H (2003) Ganoderma versus mycorrhiza. Oil Palm Bull 47:6–14

    Google Scholar 

  • Baniasadi F, Shahidi Bonjar GH, Baghizadeh A, Karimi Nik A, Jorjandi M, Aghighi S, Rashid Farokhi P (2009) Biological control of Scleroctinia sclerotiorum, causal agent of sunflower head and stem rot disease, by use of soil borne actinomycetes isolates. Am J Agri BioSci 4(2):146–151

    Google Scholar 

  • Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57(2):535–538

    CAS  Google Scholar 

  • Cao L, Qiu Z, Dai X, Tan H, Lin Y, Zhou S (2004) Isolation of endophytic actinomycetes from roots and leaves of banana (Musa acuminata) plants and their activity against Fusarium oxysporum f. sp. cubense. World. J Microbiol Biotechnol 20:501–504

    Article  CAS  Google Scholar 

  • Crawford LD, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Appl Environ Microbiol 59(11):3899–3905

    CAS  Google Scholar 

  • Ebrahimi-Zarandi M, Shahidi Bonjar GH, Padasht Dehkaei F, Ayatollahi Moosavi SA, Rashid Farokhi P, Aghighi S (2009) Biological control of rice blast (Magnaporthe oryzae) by use of Streptomyces sindeneusis isolate 263 in greenhouse. Am J Appl Sci 6:194–199

    Article  Google Scholar 

  • Elson MK, Schisler DA, Bothast RJ (1997) Selection of microorganisms for biological control of silver scurf (Helminthosporium solani) of potato tubers. Plant Dis 81:647–652

    Article  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 J Microbiol Biotechnol 23(11):1503–1509

    Article  CAS  Google Scholar 

  • Franco-Correa M, Quintana A, Duque C (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45:209–217

    Article  Google Scholar 

  • Getha K, Vikineswary S (2002) Antagonistic effects of Streptomyces violaceus niger strain G10 on Fusarium oxysporum f. sp. cubense race 4: indirect evidence for the role of antibiosis in the antagonistic process. J Ind Microbiol Biotechnol 28:303–310

    Article  CAS  Google Scholar 

  • Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research, 2nd edn. Wiley, New York

    Google Scholar 

  • Gooday GW, Zhu WY, O’Donnell RW (1992) What are the roles of chitinase in the growing fungus? FEMS Microbiol Lett 100(1–3):387–391

    Article  CAS  Google Scholar 

  • Gopalakrishnan S, Vadlamudi S, Apparla S, Bandikinda P, Vijayabharathi R, Bhimineni RK, Rupela O (2013) Evaluation of Streptomyces spp. for their plant-growth-promotion traits in rice. Can J Microbiol 59(8):534–539

    Article  CAS  Google Scholar 

  • Gopalakrishnan S, Vadlamudi S, Bandikinda P, Sathya A, Vijayabharathi R, Rupela O, Kudapa B, Katta K, Varshney RK (2014) Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiol Res 169:40–48

    Article  CAS  Google Scholar 

  • Hu QP, Xu JG (2011) A simple double-layered chrome azurol S agar (SD-CASA) plate assay to optimize the production of siderophores by a potential biocontrol agent Bacillus. Afr J Microbiol Res 5(25):4321–4327

    CAS  Google Scholar 

  • Idris AS (2011) Biology, detection and control of Ganoderma in oil palm. In: Basri MW, Choo YM, Chan KW (eds) Further advances in oil palm research (2000–2010-Volume 1). MPOB, Malaysia, pp 521–845

    Google Scholar 

  • Idris AS (2012) Latest research and management of Ganoderma disease in oil palm. In: Proceedings of the Fourth IOPRI-MPOB International Seminar: Existing and Emerging Pests and Diseases of Oil Palm Advances in Research and Management. Bandung, Indonesia, pp. 1–23

  • Idris AS, Kushairi D, Ariffin D, Basri MW (2006) Technique for inoculation of oil palm germinated seeds with Ganoderma. MPOB Inf Ser 314:1–4

    Google Scholar 

  • Idris AS, Mior MHAZ., Maizatul SM, Kushairi A (2011) Survey on status of Ganoderma disease of oil palm in Malaysia 2009–2010. In: Proceedings of the PIPOC 2011 International Palm Oil Congress (Agriculture, Biotechnology and Sustainability), Kuala Lumpur, Malaysia. MPOB Publishing, pp. 235–238

  • Ilic SB, Konstantinovic SS, Todorovic ZB, Lazic ML, Veljkovic VB, Jokovic N, Radovanovic BC (2007) Characterization and antimicrobial activity of the bioactive metabolites in streptomycete isolates. Mikrobiologiia 76(4):478–480

    Google Scholar 

  • Intra B, Mungsuntisuk I, Nihira T, Igarashi Y, Panbangred W (2011) Identification of actinomycetes from plant rhizospheric soils with antagonist activity against Colletotrichum spp., the causative agent of anthracnose disease. BMC Res Notes 4:98

    Article  CAS  Google Scholar 

  • Izzati NMZ, Abdullah F (2008) Disease suppression in Ganoderma-infected oil palm seedlings treated with Trichoderma harzianum. Plant Prot Sci 44(3):101–107

    Google Scholar 

  • Katznelson H, Bose B (1959) Metabolic activity and phosphate-dissolving capability of bacterial isolates from wheat roots, rhizosphere, and non-rhizosphere soil. Can J Microbiol 5(1):79–85

    Article  CAS  Google Scholar 

  • Khamna S, Yokata K, Pebery JF, Lumyong S (2009) Antifungal activity of Streptomyces spp. isolated from rhizosphere of Thai medicinal plants. Int J Integr Biol 6:143–147

    CAS  Google Scholar 

  • Kim YS, Lee IK, Yun BS (2015) Antagonistic effect of Streptomyces sp. BS062 against Botrytis diseases. Mycobiology 43(3):39–342

    Google Scholar 

  • Kolombet LV, Zhigletsova SK, Kosareva NI, Bystrova EV, Derbyshev VV, Krasnova SP, Schisler D (2008) Development of an extended shelf-life, liquid formulation of the biofungicide Trichoderma asperellum. World J Microbiol Biotechnol 24:123–131

    Article  Google Scholar 

  • Kustner E (1968) The actinomycetes. In: Burges A, Raw F (eds) Soil biology. Academic Press, London, pp 111–124

    Google Scholar 

  • Larralde-Corona CP, Santiago-Mena MR, Sifuentes-Rincon AM, Rodriguez-Luna IC, Rodriguez-Perez MA, Shirai K, Narvaez-Zapata JA (2008) Biocontrol potential and polyphasic characterization of novel native Trichoderma strains against Macrophomina phaseolina isolated from sorghum and common bean. Appl Microbiol Biotechnol 80:167–177

    Article  CAS  Google Scholar 

  • Lo CW, Lai NS, Cheah HY, Wong NKI, Ho CC (2002) Actinomycetes isolated from soil samples from the Crocker Range Sabah. ASEAN Rev Biodiver Environ Conserv 9:1–7

    Google Scholar 

  • Lyons AJ, Pridham TG (1965) Colorimetric determination of color of aerial mycelium of Streptomycetes. J Bacteriol 89:159–169

    Google Scholar 

  • Maizatul Suriza M, Idris AS (2009) Nursery evaluation of Agrobacterium radiobacter, Burkholderia cepacia and Pseudomonas syringae to control Ganoderma boninense infection in oil palm. In Proceedings of Agriculture, Biotechnology and Sustainability Conference Volume 3. PIPOC 2009-International Palm Oil Congress: Kuala Lumpur, Malaysia. MPOB Publishing

  • Merckx R, Dijkstra A, Den Hartog A, Van Veen JA (1987) Production of root-derived material and associated microbial growth in soil at different nutrient levels. Biol Fertil Soils 5(2):126–132

    Article  Google Scholar 

  • Mutitu EW, Muiru WM, Mukunya DM (2008) Evaluation of antibiotic metabolites from actinomycete isolates for the control of late blight of tomatoes under greenhouse conditions. Asian J Plant Sci 7:284–290

    Article  Google Scholar 

  • Nur Azura AB, Yusoff M, Tan GYA, Jegadeesh R, Appleton DR, Vikineswary S (2016) Streptomyces sanglieri which colonised and enhanced the growth of Elaeis guineensis Jacq. seedlings was antagonistic to Ganoderma boninense in in vitro studies. J Ind Microbiol Biotechnol 43(4):485–493

    Article  CAS  Google Scholar 

  • Nurrashyeda R, Idris AS, Madihah AZ, Ramle M, Kushairi A (2011) Hendersonia GanoEF1 granules for the control of Ganoderma boninense in oil palm. MPOB Information Series, No. 556. MPOB TT No. 483

  • Nurrashyeda R, Maizatul SM, Idris AS, Madihah AZ, Nasyaruddin M (2016) The potential of endophytic bacteria as a biological control agent for Ganoderma disease in oil palm. Sains Malays 45(3):401–409

    Google Scholar 

  • Oskay M (2009) Antifungal and antibacterial compounds from Streptomyces strains. Afr J Biotechnol 8(13):3007–3017

    CAS  Google Scholar 

  • Pattanapipitpaisal P, Kamlandharn R (2012) Screening of chitinolytic actinomycetes for biological control of Sclerotium rolfsii stem rot disease of chilli. Songklanakarin J Sci Technol 34

  • Prapagdee B, Kuekulvong C, Mongkolsuk S (2008) Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. Int J Biol Sci 4(5):330–337

    Article  CAS  Google Scholar 

  • Pridham TG (1965) Color and Streptomycetes—report of an International Workshop on Determination of Color of Streptomycetes. Appl Environ Microbiol 1:43–61

    Google Scholar 

  • Sabaratnam S, Traquair JA (2002) Formulation of Streptomyces biological control agent for the suppression of Rhizoctonia damping-off in tomato transplant. Biocontrol 23(3):245–252

    CAS  Google Scholar 

  • Sahilah AM, Tang SY, Zaimawati MN, Rosnah H, Kalsum MU, Son R (2010) Identification and characterization of actinomycetes for biological control of bacterial wilt of Ralstonia solanacearum isolated from tomato. J Trop Agric Food Sci 38(1):103–114

    Google Scholar 

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

    CAS  Google Scholar 

  • Sardi P, Saracchi M, Quaroni S, Petrolini B, Borgonovi GE, Merli S (1992) Isolation of endophytic Streptomyces strains from surface-sterilized roots. Appl Environ Microbiol 58:2691–2693

    CAS  Google Scholar 

  • Sariah M, Zakaria K (2000) The use of soil amendments for the control of basal stem rot of oil palm seedling. In: Flood J, Bridge PD, Holderness M (eds) Ganoderma diseases in perennial crops. CABI Publishing, Wallingford, pp 88–99

    Google Scholar 

  • Sariah M, Choo CW, Zakaria H, Norihan MS (2005) Quantification and characterization of Trichoderma spp. from different ecosystems. Mycopathologia 159:113–117

    Article  CAS  Google Scholar 

  • Saxena S, Pandey AK (2001) Microbial metabolites as eco-friendly agrochemicals for the next millennium. Appl Microbiol Biotechnol 55(4):395–403

    Article  CAS  Google Scholar 

  • Shahrokhi S, Shahidi Bonjar GH, Saadoun I (2005) Biological control of potato isolate of Rhizoctonia solani by Streptomyces olivaceus strain 115. Biotechnology 4(2):132–138

    Article  Google Scholar 

  • Shariffah-Muzaimah SA, Idris AS, Madihah AZ, Dzolkhifli O, Kamaruzzaman S, Cheong PCH (2015) Isolation of actinomycetes from rhizosphere of oil palm (Elaeis guineensis Jacq.) for antagonism against Ganoderma boninense. J Oil Palm Res 27:19–29

    Google Scholar 

  • Shen T, Wang C, Yang H, Deng Z, Wang S, Shen B, Shen Q (2016) Identification, solid-state fermentation and biocontrol effects of Streptomyces hygroscopicus B04 on strawberry root rot. Appl Soil Ecol 103:36–43

    Article  Google Scholar 

  • Shimizu M, Nakagawa Y, Sato Y, Furumai T, Igarashi Y, Onaka H, Yoshida R, Kunoh H (2000) Studies on endophytic actinomycetes (I) Streptomyces sp. isolated from Rhododendron and its antifungal activity. J Gen Plant Pathol 66(4):360–366

    Article  CAS  Google Scholar 

  • Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  • Singh G (1991) Ganoderma—the scourge of oil palm in the coastal areas. The Planter 67:421–444

    Google Scholar 

  • Singh PP, Shin YC, Park CS, Chung YR (1999) Biological controls of Fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89:92–99

    Article  CAS  Google Scholar 

  • Sousa CS, Soares ACF, Garrido MS (2008) Characterization of Streptomycetes with potential to promote plant growth and biocontrol. Sci Agric 65:50–55

    Article  Google Scholar 

  • Sundram S, Abdullah F, Ahmad ZAM, Yusuf UK (2008) Efficacy of single and mixed treatments of Trichoderma harzianum as biocontrol agents of Ganoderma basal stem rot in oil palm. J Oil Palm Res 20:470–483

    Google Scholar 

  • Sundram S, Meon S, Seman IA, Othman R (2015) Application of arbuscular mycorrhizal fungi with Pseudomonas aeruginosa UPMP3 reduces the development of Ganoderma basal stem rot disease in oil palm seedlings. Mycorrhiza 25(5):387–397

    Article  CAS  Google Scholar 

  • Susanto A, Sudharto PS, Purba RY (2005) Enhancing biological control of basal stem rot disease (Ganoderma boninense) in oil palm plantations. Mycopathologia 159:153–157

    Article  CAS  Google Scholar 

  • Taechowisan T, Lumyong S (2003) Activity of endophytic actinomycetes from roots of Zingiber officinale and Alpinia galangal against phytopathogenic fungi. Ann Microbiol 53(3):291–298

    Google Scholar 

  • Tahvonen RT (1988) Microbial control of plant diseases with Streptomyces spp. EPPO Bull 18(1):55–59

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  Google Scholar 

  • Tan CJ, How KC, Loh-Mia PP, Ismet A, Getha K, Seki T, Vikineswary S (2002) Bioactivity of selected actinomycetes against Ganoderma boninense. Asia Pacific J Mol Biol Biotechnol 10:119–125

    CAS  Google Scholar 

  • 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(5):2161–2171

    Article  CAS  Google Scholar 

  • Waksman SA (1959) The Actinomycetes. vol. I. Nature, occurrence and activities. The Williams & Wilkins Company, Baltimore

    Google Scholar 

  • Xiao K, Kinkel LL, Samac DA (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol Control 23(3):285–295

    Article  CAS  Google Scholar 

  • Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 61(8):3119–3128

    CAS  Google Scholar 

  • Zaiton S, Sariah M, Ahmad ZAM (2008) Effect of endophytic bacteria on growth and suppression of Ganoderma boninense infection in oil palm. Int J Agric Biol 10:127–132

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biology Research Division, Ganoderma and Diseases Research for Oil Palm (GanoDROP) Unit, Malaysian Palm Oil Board, 6 Persiaran Institusi, Bandar Baru Bangi, 43000, Kajang, Selangor, Malaysia

    S. A. Shariffah-Muzaimah, A. S. Idris, A. Z. Madihah & M. Maizatul-Suriza

  2. Plant Protection Department, Faculty of Agriculture, Universiti Putra Malaysia, 43400, Serdang, Malaysia

    O. Dzolkhifli & S. Kamaruzzaman

Authors
  1. S. A. Shariffah-Muzaimah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. S. Idris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Z. Madihah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. Dzolkhifli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Kamaruzzaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Maizatul-Suriza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. A. Shariffah-Muzaimah.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shariffah-Muzaimah, S.A., Idris, A.S., Madihah, A.Z. et al. Characterization of Streptomyces spp. isolated from the rhizosphere of oil palm and evaluation of their ability to suppress basal stem rot disease in oil palm seedlings when applied as powder formulations in a glasshouse trial. World J Microbiol Biotechnol 34, 15 (2018). https://doi.org/10.1007/s11274-017-2396-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-017-2396-1

Keywords

Search

Navigation