* Corresponding Author
Isolation, Identification and the Abilities of Fungi Associated with Agarwood from Bangka Belitung Island to Induce Agarwood Compounds
https://doi.org/10.22146/jpti.31623 Hartono Hartono(1), Arif Wibowo(2), Achmadi Priyatmojo(3*)
(1) Department of Agriculture of Bangka Tengah Jln. Titian Puspa II Komplek Terpadu Pemda Kabupaten Bangka Tengah 33681 Indonesia
(2) Department of Plant Protection, Faculty of Agriculture, Universitas Gadjah Mada Jln. Flora No. 1, Bulaksumur, Sleman, Yogyakarta 55281
(3) Department of Plant Protection, Faculty of Agriculture, Universitas Gadjah Mada Jln. Flora No. 1, Bulaksumur, Sleman, Yogyakarta 55281
(*) Corresponding Author
Abstract
Agarwood is one of the non-timber forest products that have high economic value. Agarwood is widely used to make incense, perfume and other products. Sapwood on agarwood is a group of secondary metabolites of agarwood plants that form a lump and have a certain color and aroma. The fragrant aroma of sapwood on agarwood is formed due to pathogenic infection of the agarwood tree. Until now, most studies of fungi forming sapwood are only oriented to virulent pathogenic fungi in nature and have never been reported to form hypovirulent agarwood. This study aimed to evaluate the potential of fungi originating from sapwood on agarwood especially those that are hypovirulent in inducing sesquiterpene compounds. This study included exploration, isolation, identification, and induction of fungi associated with sapwood on agarwood from four districts in the Bangka Belitung Islands Province. Hypovirulence test in cucumber sprouts and sesquiterpene induction test on agarwood plantlets was conducted in the laboratory. Based on the isolation results, 48 fungal isolates associated with sapwood on agarwood were found: fungi of genus Fusarium, Trichoderma, Aspergillus, Penicillium, Curvularia, Peniophora, and six isolates were unidentified. Based on the hypovirulence test on cucumber sprouts, 46 isolates of the fungus 46 isolates were virulent and 2 isolates were hypovirulent (isolates 4A and 17A). The induction of sesquiterpene compounds on the agarwood plant was employed using 5 sample isolates consisting of 4 virulent isolates (2A, 7A, 18A, and 25A) and 1 hypovirulent isolate (Isolate 4A). The results showed that hypovirulent isolates were able to produce sesquiterpenes even in small amounts compared with virulent isolates. Isolates produced many sesquiterpene compounds were isolates 18A (Fusarium sp.). Sesquiterpene compounds formed were pinene, terpineol, patchouli alcohol, trimethyl-naphthalene, beta-caryophyllene, camphor, eugenol, trimethyl- benzene, phenanthrene, citronella, eucalyptol, 4-hydroxy-4-methyl-2-pentanone. In this study also found fungi associated with sapwood on agarwood which had never been reported by previous researchers, Peniophora sp. (isolate 25A).
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Ali, N.A.M., N. Ismail, & M.N. Taib. 2012. Analysis of Agarwood Oil (Aquilaria malaccensis) Based on GC-MS Data, p. 470−473. In IEEE (ed.), Signal Processing and its Applications (CSPA), 2012 IEEE 8th International Colloquium on Signal Processing and its Applications .
Azzarina, A. B., R. Mohamed, S. Y. Lee, & M. Nazre. 2016. Temporal and Spatial Expression of Terpene Synthase Genes Associated with Agarwood Formation in Aquilaria malaccensis. New Zealand Journal of Forestry Science 46: 1−13.
Baidyaroy, D., G. Hausner, M. Hafez, F. Michel, D. W. Fulbright, & H. Bertrand. 2011. A 971-bp Insertion in the rns Gene is Associated with Mitochondrial Hypovirulence in a Strain of Cryphonectria parasitica Isolated from Nature. Fungal Genetics and Biology 48: 775−783.
Barnett, H.L. & B.B. Hunter. 1998. Illustrated Genera of Imperfect Fungi 4rd ed. APS Press, St. Paul, Minnesota. 218 p.
Cardoso, J.E., & E. Echandi. 1987. Biological Control of Rhizoctonia Root Rot of Snap Bean with Binucleate Rhizoctonia-like Fungi. Plant Disease 71: 167−170.
Castro, M., K. Kramer, L. Valdivia, S. Ortiz, & A. Castillo. 2003. A Double-Stranded RNA Mycovirus Confers Hypovirulence-associated Traits to Botrytis cinerea. FEMS Microbiology Letters 228: 87−91.
Chen, H., Y. Yang, J. Xue, J. Wei, Z. Zhang, & H. Chen. 2011. Comparison of Compositions and Antimicrobial Activities of Essential Oils from Chemically Stimulated Agarwood, Wild Agarwood and Healthy Aquilaria sinensis (Lour.) Gilg Trees. Molecules 16: 4884−4896.
Chhipa, H. & N. Kaushik. 2017. Fungal and Bacterial Diversity Isolated from Aquilaria malaccensis Tree and Soil, Induces Agarospirol Formation within 3 Months after Artificial Infection. Frontiers in Microbiology 8: 1−12.
Chu, Y.M., J.J. Jeon, S.J. Yea, Y.H. Kim, S.H. Yun, Y.W. Lee & K.H. Kim. 2002. Double-Stranded RNA Mycovirus from Fusarium graminearum. Applied and Environmental Microbiology 68: 2529−2534.
Cui, J., C. Wang, S. Guo, L. Yang, P. Xiao, & M. Wang. 2013a. Evaluation of Fungus-Induced Agilawood from Aquilaria sinensis in China. Symbiosis 60: 37−44.
Cui, J.L., C.L. Wang, S.X. Guo, P.G. Xiao, & M.L. Wang. 2013b. Stimulation of Dragon’s Blood Accumulation in Dracaena cambodiana via Fungal Inoculation. Fitoterapia 87: 31−36.
Dahham, S., Y. Tabana, D. Sandai, M. Ahmed, & A. Majid. 2016. In Vitro Anti-Cancer and Anti- Angiogenic Activity of Essential Oils Extracts from Agarwood (Aquilaria crassna). Medicinal & Aromatic Plants 5: 1−10.
Darissa, O., G. Adam, & W. Schäfer. 2012. A dsRNA Mycovirus Causes Hypovirulence of Fusarium graminearum to Wheat and Maize. European Journal of Plant Pathology 134: 181−189.
Darissa, O., P. Willingmann, W. Schafer, & G. Adam. 2011. A Novel Double-Stranded RNA Mycovirus from Fusarium graminearum: Nucleic Acid Sequence and Genomic Structure. Archives of Virology 156: 647−658.
Dou, D. & J.-M. Zhou. 2012. Phytopathogen Effectors Subverting Host Immunity: Different Foes, Similar Battleground. Cell Host & Microbe 12: 484−495.
Faizal, A., R. R. Esyanti, E. N. Aulianisa, E. Santoso, & M. Turjaman. 2017. Formation of Agarwood from Aquilaria malaccensis in Response to Inoculation of Local Strains of Fusarium solani. Trees 31: 189−197.
Gunasekera, S.P., A.D. Kinghorn, G.A. Cordell, & N.R. Farnsworth. 1981. Plant Anticancer Agents. XIX. Constituents of Aquilaria malaccensis. Journal of Natural Products 44: 569−572.
Hashim, Y. Z. H.-Y., N. I. Ismail, & P. Abbas. 2014a. Analysis of Chemical Compounds of Agarwood Oil from Different Species by Gas Chromatography Mass Spectrometry (GCMS). IIUM Engineering Journal 15: 55−60.
Hashim, Y. Z. H.-Y., A. Phirdaous, & A. Azura. 2014b. Screening of Anticancer Activity from Agarwood Essential Oil. Pharmacognosy Research 6: 191−194.
Ibrahim, A., S. Al-Rawi, A. A. Majid, N. A. Rahman, K. Abo-Salah, & M. Ab Kadir. 2011. Separation and Fractionation of Aquilaria malaccensis Oil Using Supercritical Fluid Extraction and the Cytotoxic Properties of the Extracted Oil. Procedia Food Science 1: 1953−1959.
Ismail, N., M.A.N. Azah, M. Jamil, M.H.F. Rahiman, S.N. Tajuddin, & M.N. Taib. 2013. Analysis of High Quality Agarwood oil Chemical Compounds by Menas SPMEGC-MS and Z-Score Technique. Malaysian Journal of Analytical Sciences 17: 403−413.
Jayaraman, S., & R. Mohamed. 2015. Crude Extract of Trichoderma Elicits Agarwood Substances in Cell Suspension Culture of the Tropical Tree, Aquilaria malaccensis Lam. Turkish Journal of Agriculture and Forestry 39: 163−173.
Jong, P.L., P. Tsan, & R. Mohamed. 2014. Gas Chromatography-Mass Spectrometry Analysis of Agarwood Extracts from Mature and Juvenile Aquilaria malaccensis. International Journal of Agriculture and Biology 16: 644−648.
Juan-Abgona, R.V., N. Katsuno, K. Kageyama, & M. Hyakumachi. 1996. Isolation and Identification of Hypovirulent Rhizoctonia spp. from Soil. Plant Pathology 45: 896−904.
Kumeta, Y. & M. Ito. 2010. Characterization of δ- guaiene Synthases from Cultured Cells of Aquilaria, Responsible for the Formation of the Sesquiterpenes in Agarwood. Plant Physiology 154: 1998−2007.
Lancaster, C. & E. Espinoza. 2012. Evaluating Agarwood Products for 2-(2-phenylethyl) Chromones Using Direct Analysis in Real Time Time-of- Flight Mass Spectrometry. Rapid Communications in Mass Spectrometry 26: 2649−2656.
Lambevska, A., K. Resuvska, & M. Karadelev. 2013. New Data on the Taxonomy, Distribution and Ecology of the Genus Peniophora Cooke (Basidiomycota, Fungi) in the Republic of Macedonia. Macedonian Journal of Ecology and Environment 15: 69−79.
Lee, K.M., J. Yu, M. Son, Y.W. Lee, & K.H. Kim. 2011. Transmission of Fusarium boothii Mycovirus via Protoplast Fusion Causes Hypovirulence in Other Phytopathogenic Fungi. PLoS One 6: 1−9.
Leksonowati, A. 2016. Interaksi antara Biak Suspensi Sel Gaharu (Aquilaria malaccensis) dan Fusarium spp. dalam Menghasilkan Senyawa Seskuiterpena. Tesis. Institut Pertanian Bogor, Bogor, Jawa Barat. 63 p.
Leslie, J.F. & B.A. Summerell. 2006. The Fusarium Laboratory Manual. Blackwell Publishing, Victoria, 388p.
Liao, Y., J. Wei, Y. Xu & Z. Zhang. 2015. Cloning, Expression and Characterization of COI1 Gene (AsCOI1) from Aquilaria sinensis (Lour.) Gilg. Acta Pharmaceutica Sinica B 5: 473−481.
Machado, K.M.G., D.R. Matheus, & V.L. R. Bononi. 2005. Ligninolytic Enzymes Production and Remazol Brilliant Blue R Decolorization by Tropical Brazilian Basidiomycetes Fungi. Brazilian Journals of Microbiology 36: 246−252.
Mohamed, R., P.L. Jong, & I. Nurul Irdayu. 2014. Succession Patterns of Fungi Associated to Wound-Induced Agarwood in Wild Aquilaria malaccensis Revealed from Quantitative PCR Assay. World Journal of Microbiology and Biotechnology 30: 2427−2436.
Muslim, A., H. Horinouchi, & M. Hyakumachi. 2003. Control of Fusarium Crown and Root Rot of Tomato with Hypovirulent Binucleate Rhizoctonia in Soil and Rock Wool Systems. The American Phytophatological Society 87: 739−747.
Nurbaya, T. Kuswinanti, Baharuddin, A. Rosmana, & S. Millang. 2014. Tentative Identification of Fungal Isolates Assosiated with Aquilaria spp. from Remaining Forest Areas in Nunukan Regency, North Kalimantan. The International Asian Research Journal 2: 28−36.
Okudera, Y. & M. Ito. 2009. Production of Agarwood Fragrant Constituents in Aquilaria calli and Cell Suspension Cultures. Plant Biotechnology 26: 307−315.
Premalatha, K. & A. Kalra. 2013. Molecular Phylogenetic Identification of Endophytic Fungi Isolated from Resinous and Healthy Wood of Aquilaria malaccensis, a Red Listed and Highly Exploited Medicinal Tree. Fungal Ecology 6: 205−211.
Prospero, S., M. Conedera, U. Heiniger, & D. Rigling. 2006. Saprophytic Activity and Sporulation of Cryphonectria parasitica on Dead Chestnut Wood in Forests with Naturally Established Hypovirulence. Phytopathology 96: 1337−1344.
Qi, S.-Y., M.-L. He, L.-D. Lin, C.-H. Zhang, L.-J. Hu, & H.-Z. Zhang. 2005. Production of 2-(2 phenylethyl) Chromones in Cell Suspension Cultures of Aquilaria sinensis. Plant Cell, Tissue and Organ Culture 83: 217−221.
Ran, H., L. Liu, B. Li, J. Cheng, Y. Fu, D. Jiang, & J. Xie. 2016. Co-infection of a Hypovirulent Isolate of Sclerotinia sclerotiorum with a New Botybirnavirus and a Strain of a Mitovirus. Virology Journal 13: 92−102.
Robin, C., C. Anziani, & P. Cortesi . 2000 .Relationship between Biological Control, Incidence of Hypovirulence, and Diversity of Vegetative Compatibility Types of Cryphonectria parasitica in France. Phytopathology 90: 730−737.
Sangareswari, M., K.T. Parthiban, S.U. Kanna, L. Karthiba, & D. Saravanakumar. 2016. Fungal Microbes Associated with Agarwood Formation. American Journal of Plant Sciences 7: 1445.
Sen, S., M. Dehingia, N. C. Talukdar, & M. Khan. 2017. Chemometric Analysis Reveals Links in the Formation of Fragrant Bio-molecules during Agarwood (Aquilaria malaccensis) and Fungal Interactions. Scientific Reports 7: 44406.
Shankar, S. & S. Nill. 2015. Effect of Metal Ions and Redox Mediators on Decolorization of Synthetic Dyes by Crude Laccase from a Novel White Rot Fungus Peniophora sp.(NFCCI-2131). Applied Biochemistry and Biotechnology 175: 635−647.
Siburian, R., U. Siregar, I. Siregar, & I. Wahyudi. 2013. Identification of Anatomical Characteristics of Aquilaria microcarpa in its Interaction with Fusarium solani. Biotropia 20: 104−111.
Sneh, B. 1998. Use of Non-pathogenic or Hypovirulent Fungal Strains to Protect Plants against Closely Related Fungal Pathogens. Biotechnology Advances 16: 1−32.
Sneh, B., M. Ichielevich-Auster & I. Shomer. 1989. Comparative Anatomy of Colonization of Cotton Hypocotyls and Roots by Virulent and Hypovirulent Isolates of Rhizoctonia solani. Canadian Journal of Botany 67: 2142−2149.
Supriyanto, A. Priyatmojo, & T. Arwiyanto. 2009. Screening of PGPF for Controlling Soft Rot Disease of Aloe on Peat Land. Jurnal Perlindungan Tanaman Indonesia 15: 71−82.
Supyani. 2017. Mycoviruses, Their Development toward Biological Control Agents. Jurnal Perlindungan Tanaman Indonesia 21: 1−9.
Takemoto, H., M. Ito, T. Shiraki, T. Yagura, & G. Honda. 2008. Sedative Effects of Vapor Inhalation of Agarwood Oil and Spikenard Extract and Identification of their Active Components. Journal of Natural Medicines 62: 41−46.
Tamuli, P., P. Baruah, & R. Samanta. 2011. Enzyme Activities of Agarwood (Aquilaria malaccensis Lamk.) Stem under Pathogenesis. Journal of Spices and Aromatic Crops 17: 240−243.
Trinh, D.K., D.T. Quyen, T.T. Do, & N.M. Nghiem. 2013a. Purification and Characterization of a Novel Detergent and Organic Solvent-Resistant Endo-Beta-1,4-Glucanase from a Newly Isolated Basidiomycete Peniophora sp. NDVN01. Turkish Jorunal of Biology 37: 377−384.
Trinh, D.K., D.T. Quyen, T.T. Do, T.T.H. Nguyen, & N.M. Nghiem. 2013b. Optimization of Culture Conditions and Medium Components for Carboxymethyl Cellulase (CMCase) Production by a Novel Basidiomycete Strain Peniophora sp. NDVN01. Iranian Journal of Biotechnology 11: 251−259.
Wen-Jian, Z., J. Peng-Fei, D. Wen-Hua, D. Hao-Fu & M. Wen-Li. 2014. Metabolites from the Endophytic Fungus HP-1 of Chinese Eaglewood. Chinese Journal of Natural Medicines 12: 151−153.
Wetwitayaklung, P., N. Thavanapong, & J. Charoenteeraboon. 2009. Chemical Constituents and Antimicrobial Activity of Essential Oil and Extracts of Heartwood of Aquilaria crassna Obtained from Water Distillation and Supercritical Fluid Carbon Dioxide Extraction. Silpakorn University Science and Technology Journal 3: 25−33.
Wiley, J. & Sons. 1960. Introductory Mycology. New York, London Inc., United States of America, 480 p.
Wu, B., J.G. Lee, C.J. Lim, S.D. Jia, S.W. Kwon, G. S. Hwang & J.H. Park. 2012a. Sesquiterpenoids and 2-(2-Phenylethyl)-4H-chromen-4-one (= 2- (2-Phenylethyl) - 4H - 1 - benzopyran-4-one ) Derivatives from Aquilaria malaccensis Agarwood. Helvetica Chimica Acta 95: 636−642.
Wu, M., F. Jin, J. Zhang, L. Yang, D. Jiang, & G. Li. 2012b. Characterization of a Novel Bipartite Double-Stranded RNA Mycovirus Conferring Hypovirulence in the Phytopathogenic Fungus Botrytis porri. Journal of Virology 86: 6605−6619.
Xiao, X., J. Cheng, J. Tang, Y. Fu, D. Jiang, T. S. Baker, S.A. Ghabrial, & J. Xie. 2014. A Novel Partitivirus that Confers Hypovirulence on Plant Pathogenic Fungi. Journal of Virology 88: 10120−10133.
Xu, Y.H., X. Yang, Z. Zhang, L. Liang & J.H. Wei. 2013c. Cloning and Expression Analysis of HMG-CoA Reductase from Aquilaria sinensis (Lour.) Gilg]. Yao Xue Xue Bao 48: 953−959.
Xu, Y., J. Liu, L. Liang, X. Yang, Z. Zhang, Z. Gao, C. Sui, & J. Wei. 2014. Molecular Cloning and Characterization of Three cDNAs Encoding 1- deoxy-d-xylulose-5-phosphate Synthase in Aquilaria sinensis (Lour.) Gilg. Plant Physiology and Biochemistry 82: 133−141.
Yu, X., B. Li, Y. Fu, D. Jiang, S.A. Ghabrial, G. Li, Y. Peng, J. Xie, J. Cheng, J. Huang, & X. Yi. 2010. A Geminivirus-related DNA Mycovirus that Confers Hypovirulence to a Plant Pathogenic Fungus. Proceeding of National Academy of Sciences of the United States of America 107: 8387−8392.
Zhang, L., Y. Fu, J. Xie, D. Jiang, G. Li, & X. Yi. 2009. A Novel Virus that Infecting Hypovirulent Strain XG36-1 of Plant Fungal Pathogen Sclerotinia sclerotiorum. Virology Journal 6: 1−9.
Zhang, X.L., Y.Y. Liu, J.H. Wei, Y. Yang, Z. Zhang, J.Q. Huang, H. Q. Chen, & Y. J. Liu. 2012. Production of High-quality Agarwood in Aquilaria sinensis Trees via Whole-tree Agarwood-induction Technology. Chinese Chemical Letters 23: 727−730.
Zhang, Y., H.-X. Liu, W.-S. Li, M.-H. Tao, Q.-L. Pan, Z.-H. Sun, W. Ye, H.-H. Li, & W.-M. Zhang. 2017. 2-(2-Phenylethyl)chromones from Endophytic Fungal Strain Botryosphaeria rhodina A13 from Aquilaria sinensis. Chinese Herbal Medicines 9: 58−62.
Zhang, Z., X. Wang, W. Yang, J. Wang, C. Su, X. Liu, J. Li, Y. Zhao, S. Shi, & P. Tu. 2016. Five 2-(2- Phenylethyl)chromones from Sodium Chloride- Elicited Aquilaria sinensis Cell Suspension Cultures. Molecules 21: 1−7.
Zhang, Z., X.-M. Han, J.-H. Wei, J. Xue, Y. Yang, L. Liang, X.-J. Li, Q.-m. Guo, Y.-H. Xu & Z.-H. Gao. 2014. Compositions and Antifungal Activities of Essential Oils from Agarwood of Aquilaria sinensis (Lour.) Gilg Induced by Lasiodiplodia theobromae (Pat.) Griffon. & Maubl. Journal of the Brazilian Chemical Society 25: 20−26.
DOI: https://doi.org/10.22146/jpti.31623
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