Abstract
Actinomycete strain AUM 00500 was 99.5 % similar to Streptomyces sanglieri NBRC 100784T and was evaluated for antagonistic activity towards Ganoderma boninense, the causative fungus of basal stem rot of oil palm. The strain showed strong antifungal activity towards G. boninense in in vitro and SEM analysis showed various modes of inhibition of the fungus. Ethyl acetate extracts of single culture and inhibition zone of cross-plug culture by HPLC indicated that strain AUM 00500 produced two different antibiotics of the glutarimide group namely cycloheximide and actiphenol. In greenhouse trials, oil palm seed treated with spores of S. sanglieri strain AUM 00500 at 109 cfu/ml showed significant (P < 0.05) increase in oil palm seedlings growth when compared to the control. Streptomyces sanglieri strain AUM 00500 successfully colonised the epidermal surface of the roots of treated oil palm seedlings and it was recovered from root fragments plated on starch casein agar.
Similar content being viewed by others
References
Aghighi S, Shahidi Bonjar GH, Rawashdeh R, Batayneh S, Saadoun I (2004) First report of antifungal spectra of activity of Iranian actinomycetes strains against Alternaria solani, Alternaria alternate, Fusarium solani, Phytophthora megasperma, Verticillium dahliae and Saccharomyces cerevisiae. Asian J Plant Sci 3:463–471. doi:10.3923/ajps.2004.463.471
Breton F, Hasan Y, Hariadi S, Lubis Z, De Franqueville H (2006) Characterization of parameters for the development of an early screening test for basal stem rot tolerance in oil palm progenies. J Oil Palm Res 18:24–36
Cao L, Qiu Z, You J, Tan H, Zhou S (2004) Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Lett Appl Microbiol 39:425–430. doi:10.1111/j.1472-765X.2004.01606.x
Clark CA, Matthews SW (1987) Histopathology of sweet potato root infection by Streptomyces ipomoea. Phytopathology 77:1418–1423. doi:10.1094/Phyto-77-1418
Crawford DL, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycetes antagonists of a fungal root pathogen. Appl Environ Microbiol 59:3899–3905
Dalmas FR, Astarita L, DeFilippis L, Magel E, Fiedler H-P, Bauer R, Hampp R (2013) Growth inhibition of an Araucaria angustifolia (Coniferopsida) fungal seed pathogen, Neofusicoccum parvum, by soil streptomycetes. BMC Microbiol 13:168. doi:10.1186/1471-2180-13-168
De Weert S, Bloemberg GV (2006) Rhizosphere competence and the role of root colonization in biocontrol. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Netherlands, pp 317–333
El-Tarabily KA (2003) An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupin caused by Plectosporium tabacinum. Aust J Bot 51:257–266. doi:10.1071/BT02107
El-Tarabily KA, Krishnapillai S (2006) Potential of yeasts as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Mycoscience 47:25–35. doi:10.1007/s10267-005-0268-2
El-Tarabily KA, Hardy GESJ, Sivasithamparam K (2010) Performance of three endophytic actinomycetes in relation to plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber under commercial field production conditions in the United Arab Emirates. Eur J Plant Pathol 128:527–539. doi:10.1007/s10658-010-9689-7
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi:10.2307/2408678
Getha K, Vikineswary S (2002) Antagonistic effects of Streptomyces violaceusniger 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. doi:10.1038/sj/jim/7000247
Getha K, Vikineswary S, Wong WH, Seki T, Ward A, Goodfellow M (2005) Evaluation of Streptomyces sp. strain g10 for suppression of Fusarium wilt and rhizosphere colonization in pot-grown banana plantlets. J Ind Microbiol Biotechnol 32:24–32. doi:10.1007/s10295-004-0199-5
Goudjal Y, Toumatia O, Yekkour A, Sabaou N, Mathieu F, Zitouni A (2014) Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res 169:59–65. doi:10.1016/j.micres.2013.06.014
Hartley CWS (1967) The oil palm. Longman Group Limited, London
Ho CT, Khairudin H (1997) Usefulness of soil mounding treatments in prolonging productivity of prime-aged Ganoderma infected palms. Planter 73:239–244
Höltzel A, Dieter A, Schmid DG, Brown R, Goodfellow M, Beil W, Jung G, Fiedler H-P (2003) Lactonamycin Z, an antibiotic and antitumor compound produced by Streptomyces sanglieri strain AK 623. J Antibiot 56:1058–1061. doi:10.7164/antibiotics.56.1058
Ismet A, Rizwana H, Al-Othman MR, Bakir MA (2012) Studies of actinomycetes for biological control of Colletotrichum musae pathogen during post harvest anthracnose of banana. Afr J Microbiol Res 6:3879–3886. doi:10.5897/AJMR12.088
Ji XY, Zhong ZJ, Xue ST, Meng S, He WY, Gao RM, Li YH, Li ZR (2010) Synthesis and antiviral activities of synthetic Glutarimide derivatives. Chem Pharm Bull 58:1436–1441. doi:10.1248/cpb.58.1436
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. doi:10.1099/mic.0.074146-0
Jollands P (1983) Laboratory investigations on fungicides and biological agents to control three diseases of rubber and oil palm and their potential applications. Trop Pest Manag 29:33–38. doi:10.1080/09670878309370766
Kamal R, Sharma K (2014) Control of Fusarium wilt using biocontrol agent Streptomyces sp. CPP-53 isolated from compost with plant growth promoting effect on tomato under greenhouse condition. J Microbiol Antimicrob 6:97–103. doi:10.5897/JMA2014.0318
Kim BS, Moon SS, Hwang BK (1999) Isolation, antifungal activity and structure elucidation of the glutarimide antibiotic, streptimidone, produced by Micromonospora coerulea. J Agric Food Chem 47:3372–3380. doi:10.1021/jf981259s
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721. doi:10.1099/ijs.0.038075-0
Kok SM, Goh YK, Tung HJ, Goh KJ, Wong WC, Goh YK (2013) In vitro growth of Ganoderma boninense isolates on novel palm extract medium and virulence on oil palm (Elaeis guineensis) seedlings. Malays J Microbiol 9:33–42
Kornerup A, Wanscher JH (1963) Methuen handbook of colour. Methuen & Co., Ltd., London
Kortemaa H, Rita H, Haahtela K, Smolander A (1994) Root-colonization ability of antagonistic Streptomyces griseoviridis. Plant Soil 163:77–83. doi:10.1007/BF00033943
Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot B, Vanncanneyt M, Swings J, Kim SB, Liu Z, Chun J, Tamura T, Oguchi A, Kikuchi T, Kikuchi H, Nishii T, Tsuji K, Yamaguchi Y, Tase A, Takahashi M, Sakane T, Suzuki KI, Hatano K (2012) Phylogenetic study of the species within the family Streptomycetaceae. Antonie Van Leeuwenhoek 101:73–104. doi:10.1007/s10482-011-9656-0
Laila N, Umi Kalsom Y, Tan SG, Ahmad I (2013) Ecology status of Ganoderma and basal stem rot disease of oil palms (Elaies guineensis Jacq.). Aust J Crop Sci 7:1723–1727
Lakhvich FA, Buravskaya TN, Akhrem AA (1993) Synthesis of actiphenol and its normethyl analogues and 6-hydroxy derivatives. Chem Nat Compd 29:526–529. doi:10.1007/BF00630584
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175
Manfio GP, Atalan E, Zakrzewska-Czerwinska J, Mordarski M, Rodriguez C, Collins MD, Goodfellow M (2003) Classification of novel soil streptomycetes as Streptomyces aureus sp. nov., Streptomyces laceyi sp. nov. and Streptomyces sanglieri sp. nov. Antonie Van Leeuwenhoek 83:245–255. doi:10.1023/A:1023332427794
McNear DH Jr (2013) The rhizosphere-roots, soil and everything in between. Nat Educ Knowl 4:1
Mishra AK, Dutta S, Dileep-Kumar BS (2005) Effect of florescent Pseudomonas strain on crop enhancement and suppression of root diseases of tea. In: Proceedings of the Asia conference on emerging trends in plant-microbe interactions, December 8–10, 2005, University of Madras, Chennai
Nur Azura AB (2007) Colonization of selected actinomycetes on roots of oil palm seedlings and its effects on plant growth. B.Sc. Dissertation, University of Malaya, Kuala Lumpur, Malaysia
Ola ARB, Thomy D, Lai D, Brötz-Oesterhelt H, Proksch P (2013) Inducing secondary metabolite production by the endophytic fungus Fusarium tricinctum through coculture with Bacillus subtilis. J Nat Prod 76:2094–2099. doi:10.1021/np400589h
Palaniyandi SA, Yang SH, Cheng JH, Meng L, Suh J-W (2011) Biological control of anthracnose (Colletotrichum gloeosporioides) in yam by Streptomyces sp. MJM5763. J Appl Microbiol 111:443–455. doi:10.1111/j.1365-2672.2011.05048.x
Sadfi N, Chérif M, Hajlaoui MR, Boudabbous A, Bélanger R (2002) Isolation and partial purification of antifungal metabolites produced by Bacillus cereus. Ann Microbiol 52:323–337
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schrey SD, Eric E, Früh E, Fengler S, Hommel K, Horlacher N, Schulz D, Ecke M, Kulik A, Fiedler H-P, Hampp R, Tarkka MT (2012) Production of fungal and bacterial growth modulating secondary metabolites is widespread among mycorrhiza-associated streptomycetes. BMC Microbiol 12:164. doi:10.1186/1471-2180-12-164
Shahbazi P, Yusoff M, Tan GYA, Avin FA, Teo WFA, Vikineswary S (2014) In vitro and in vivo evaluation of Streptomyces suppressions against Anthracnose in chilli caused by Colletotrichum. Sains Malays 43:697–705
Shamala S, Sariah M, Idris AS, Radziah O (2015) Application of arbuscular mycorrhizal fungi with Pseudomonas aeruginosa UPMP3 reduces the development of Ganoderma basal stem rot disease in oil palm seedlings. Mycorrhiza 25:387–397. doi:10.1007/s00572-014-0620-5
Shimizu M (2011) Endophytic actinomycetes: biocontrol agents and growth promoters. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer-Verlag, Berlin, pp 201–220
Shirling EB, Gottlieb D (1966) Methods of characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340. doi:10.1099/00207713-16-3-313
Singh G (1991) Ganoderma-the scourge of oil palms in the coastal areas. Planter 67:421–444
Tahvonen R, Avikainen H (1987) The biological control of seed-borne Alternaria brassicicola of cruciferous plants with a powdery preparation of Streptomyces sp. J Agric Sci Finland 59:199–208
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092
Tan CJ, How KC, Loh-Mia PP, Ismet A, Getha K, Seki T, Vikineswary S (2002) Bioactivity of selected actinomycetes against Ganoderma boninense. Asia Pac J Mol Biol Biotechnol 10:119–125
Tan GYA, Ward AC, Goodfellow M (2006) Exploration of Amycolatopsis diversity in soil using genus-specific primers and novel selective media. Syst Appl Microbiol 29:557–569. doi:10.1016/j.syapm.2006.01.007
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-spesific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673
Turner PD (1981) Oil palm diseases and disorders. Oxford University Press, Oxford
Acknowledgments
The authors would like to thank the University of Malaya for Grants (PS189/2008B) and (J-21001-76536). The authors also thank the Applied Agricultural Resources Sdn. Bhd. (for the seeds) and Sime Darby Plantation Sdn. Bhd. (for Ganoderma boninense culture) used in this study. Mr. Roslee Halip is thanked for his assistance with SEM.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nur Azura, A.B., Yusoff, M., Tan, G.Y.A. et al. 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, 485–493 (2016). https://doi.org/10.1007/s10295-015-1724-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10295-015-1724-4