Fungi mediated agarwood (A. malaccensis) production and their pharmaceutical applications: A systematic review

Abstract

Aquilaria malaccensis is a tropical tree that produces expensive resinous heartwood agarwood through the natural process induced by natural or artificial injury or microbial infection. Fungi are commonly noticed as the main microbial component responsible for agarwood formation. The current review investigated the agarwood quality and fungi diversity in artificial and natural agarwood from A. malecensis trees from the rainforest for various pharmaceutical applications. Apart from being an aromatherapy material, in medicinal prospect, agarwood can be used as a carminative, stimulant for heart palpitation, tonic during pregnancy, remedy during the post-natal recovery period, and cure for the disease of the female genital part. The whitebark of agarwood is believed to heal jaundice and body pain. Moreover, agarwood helps to relieve body pain, warm the abdomen, relieve asthma, treat coughs, and acroparalysis acts as antihistamine, analgesic and anti-inflammatory. In Chinese traditional medicine, it is helpful as a sedative to relieve gastric problems, relieve rheumatism and high fever. Agarwood properties were able to fight cancer cells but very little is known about this process. The present review also illustrated the variety of kinds of pharmaceutical applications in the treatment of various diseases. Current review findings proved that artificial agarwood may produce quality equal to natural agarwood and may not be affected by fungi interacting with the tree, which can be used as a superior pharmaceutical application.

Keywords

• Agarwood
• Aquilaria malaccensis
• Inoculation
• Pharmaceutical applications

Kaynakça

1. Akter, S., Islam, M.T., Zulkefeli, M., Khan, S.I., 2013. Agarwood production-a multidisciplinary field to be explored in Bangladesh. International Journal of Pharmaceutical and Life Sciences, 2(1), 22-32.
2. Ali, N.A.M., Jin, C.B., Jamil, M., 2016. Agarwood (Aquilaria malaccensis) Oils Essential Oils in Food Preservation, Flavor and Safety (pp.173-180): Elsevier.
3. Anastasaki, E., Kanakis, C., Pappas, C., Maggi, L., Del Campo, C.P., Carmona, M., Polissiou, M.G., 2009. Geographical differentiation of saffron by GC–MS/FID and chemometrics. European Food Research and Technology, 229(6), 899-905.
4. Angelova, Z., Georgiev, S., Roos, W., 2006. Elicitation of plants. Biotechnology & Biotechnological Equipment, 20(2), 72-83.
5. Antonopoulou, M., Compton, J., Perry, L.S., Al-Mubarak, R., 2010. The trade and use of agarwood (Oudh) in the United Arab Emirates. TRAFFIC Southeast Asia, Petaling Jaya, Selangor, Malaysia.
6. Arthur, C.L., Pawliszyn, J., 1990. Solid phase microextraction with thermal desorption using fused silica optical fibers. Analytical Chemistry, 62(19), 2145-2148.
7. Barden, A., Anak, N.A., Mulliken, T., Song, M., 2000. Heart of the matter: agarwood use and trade and CITES implementation for Aquilaria malaccensis. TRAFFIC International, Cambridge, UK.
8. Bednarek, P., 2012. Chemical warfare or modulators of defence responses–the function of secondary metabolites in plant immunity. Current Opinion in Plant Biology, 15(4), 407-414.

9. Bhuiyan, M.N.I., Begum, J., Bhuiyan, M.N.H., 2009. Analysis of essential oil of eaglewood tree (Aquilaria agallocha Roxb.) by gas chromatography mass spectrometry. Bangladesh Journal of Pharmacology, 4(1), 24-28.
10. Chakrabarti, K., Kumar, A., Menon, V., 1994. Trade in agarwood: TRAFFIC-India, WWF, India.
11. Chamorro, E.R., Zambón, S.N., Morales, W.G., Sequeira, A.F., Velasco, G.A., 2012. Study of the chemical composition of essential oils by gas chromatography. Gas Chromatography in Plant Science, Wine Technology, Toxicology and Some Specific Applications, 1, 307-324.
12. Charry‐Parra, G., DeJesus‐Echevarria, M., Perez, F.J., 2011. Beer volatile analysis: optimization of HS/SPME coupled to GC/MS/FID. Journal of Food Science, 76(2), C205-C211.
13. Chehri, K., Salleh, B., Zakaria, L., 2015. Morphological and phylogenetic analysis of Fusarium solani species complex in Malaysia. Microbial Ecology, 69(3), 457-471.
14. Chen, H., Yang, Y., Xue, J., Wei, J., Zhang, Z., Chen, H., 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(6), 4884-4896.
15. Chitre, T., Bhutada, P., Nandakumar, K., Somani, R., Miniyar, P., Mundhada, Y., Jain, K., 2007. Analgesic and anti-inflammatory activity of heartwood of Aquilaria agallocha in laboratory animals. Pharmacol Online, 1, 288-298.
16. Chua, L.S.L., 2008. Agarwood (Aquilaria malaccensis) in Malaysia. Forest Research Institute Malaysia.
17. Cui, J., Wang, C., Guo, S., Yang, L., Xiao, P., Wang, M., 2013. Evaluation of fungus-induced agilawood from Aquilaria sinensis in China. Symbiosis, 60(1), 37-44.
18. Dahham, S.S., Ahamed, M.B.K., Saghir, S.M., Alsuede, F.S., Iqbal, M.A., Majid, A.M.S.A., 2014. Bioactive essential oils from Aquilaria crassna for cancer prevention and treatment. Global Journal on Advances Pure and Applied Sciences, 4, 26-31.
19. Degenhardt, J., 2009. Indirect defense responses to herbivory in grasses. Plant Physiology, 149(1), 96-102.
20. Duriyaprapan, S., Khuankhamnuan, C., Tanpanich, S., 2003. The plant resources of south-east Asia (PROSEA). In III WOCMAP Congress on Medicinal and Aromatic Plants-Volume 1: Bioprospecting and Ethnopharmacology 675 (pp. 15-21).
21. Elias, M.F., Ibrahim, H., Mahamod, W.R.W., 2017. A review on the malaysian Aquilaria species in karas plantation and agarwood production. International Journal of Academic Research in Business and Social Sciences, 7(4), 1021-1029.
22. Frey, M., Schullehner, K., Dick, R., Fiesselmann, A., Gierl, A., 2009. Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants. Phytochemistry, 70(15-16), 1645-1651.
23. Frost, C.J., Mescher, M.C., Carlson, J.E., De Moraes, C.M., 2008. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiology, 146(3), 818-824.
24. Gunn, B., Stevens, P., Singadan, M., Sunari, L., Chatterton, P., 2004. Eaglewood in Papua New Guinea.
25. Hafizi, R., Salleh, B., Latiffah, Z., 2013. Morphological and molecular characterization of Fusarium solani and F. oxysporum associated with crown disease of oil palm. Brazilian Journal of Microbiology, 44, 959-968.
26. Hendra, H., Moeljopawiro, S., Nuringtyas, T.R., 2016. Antioxidant and antibacterial activities of agarwood (Aquilaria malaccensis Lamk.) leaves. In AIP Conference Proceedings (Vol. 1755, No. 1, p. 140004). AIP Publishing LLC.
27. Heuveling van Beek, H., Phillips, D., 1999. Agarwood: trade and CITES implementation in Southeast Asia. Unpublished report prepared for TRAFFIC Southeast Asia, Malaysia.
28. Holm, T., 1999. Aspects of the mechanism of the flame ionization detector. Journal of Chromatography A, 842(1-2), 221-227.
29. Huang, M., Sanchez‐Moreiras, A.M., Abel, C., Sohrabi, R., Lee, S., Gershenzon, J., Tholl, D., 2012. The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)‐β‐caryophyllene, is a defense against a bacterial pathogen. New Phytologist, 193(4), 997-1008.
30. Hübschmann, H.J., 2015. Handbook of GC-MS: fundamentals and applications. John Wiley & Sons.
31. Inskipp, T., Gillett, H.J., 2005. Checklist of CITES species and annotated CITES appendices and reservations: a reference to the appendices to the Convention on International Trade in Endangered Species of Wild Fauna and Flora: United Nations Envir Programme.
32. Ismail, N., Rahiman, M.H.F., Taib, M.N., Ibrahim, M., Zareen, S., Tajuddin, S.N., 2016. Observation on SPME different headspace fiber coupled with GC-MS in extracting high quality agarwood chipwood. IEEE International Conference on Automatic Control and Intelligent Systems (I2CACIS) (pp. 214-218).
33. Jayachandran, K.S.I.P., Sekar, I., Parthiban, K.T., Amirtham, D., Suresh, K.K., 2014. Analysis of different grades of agarwood (Aquilaria malaccensis Lamk.) oil through GC-MS. Indian Journal of Natural Products and Resources, 5(1), 44-47.
34. Jensen, A., 2009. Valuation of non-timber forest products value chains. Forest Policy and Economics, 11(1), 34-41.
35. Jensen, A., Meilby, H., 2010. Returns from Harvesting a Commercial Non-timber Forest Product and Particular Characteristics of Harvesters and Their Strategies: Aquilaria crassna and Agarwood in Lao PDR1. Economic Botany, 64(1), 34-45.
36. Jung, D., 2011. The value of agarwood. Reflections upon its use and history in South Yemen.
37. Jung, D., 2013. The Cultural Biography of Agarwood–Perfumery in Eastern Asia and the Asian Neighbourhood1. Journal of the Royal Asiatic Society, 23(1), 103-125.
38. Kenmotsu, Y., Ogita, S., Katoh, Y., Yamamura, Y., Takao, Y., Tatsuo, Y., Kurosaki, F., 2011. Methyl jasmonate-induced enhancement of expression activity of Am-FaPS-1, a putative farnesyl diphosphate synthase gene from Aquilaria microcarpa. Journal of Natural Medicines, 65(1), 194-197.
39. Khan, A.L., Hamayun, M., Kim, Y.H., Kang, S.M., Lee, J.H., Lee, I.J., 2011. Gibberellins producing endophytic Aspergillus fumigatus sp. LH02 influenced endogenous phytohormonal levels, isoflavonoids production and plant growth in salinity stress. Process Biochemistry, 46(2), 440-447.
40. Lee, S.S., 2012. Checklist of fungi of Malaysia: Forest Research Institue Malaysia.
41. Leslie, J.F., Summerell, B.A., 2006. The fusarium laboratory manual. Ames, Iowa: Blackwell Publishing CrossRef Google Scholar, 388.
42. Li, X.J., Zhang, Q., Zhang, A.L., Gao, J.M., 2012. Metabolites from Aspergillus fumigatus, an endophytic fungus associated with Melia azedarach, and their antifungal, antifeedant, and toxic activities. Journal of Agricultural and Food Chemistry, 60(13), 3424-3431.
43. Liu, Y.Y., Wei, J.H., Gao, Z.H., Zhang, Z., Lyu, J.C., 2017. A review of quality assessment and grading for agarwood. Chinese Herbal Medicines, 9(1), 22-30.
44. Maffei, M.E., 2010. Sites of synthesis, biochemistry and functional role of plant volatiles. South African Journal of Botany, 76(4), 612-631.
45. Maggi, F., Papa, F., Cristalli, G., Sagratini, G., Vittori, S., 2010. Characterisation of the mushroom-like flavour of Melittis melissophyllum L. subsp. melissophyllum by headspace solid-phase microextraction (HS-SPME) coupled with gas chromatography (GC–FID) and gas chromatography–mass spectrometry (GC–MS). Food Chemistry, 123(4), 983-992.
46. Mei, W.L., Yang, D.L., Wang, H., Yang, J.L., Zeng, Y.B., Guo, Z.K., Dai, H.F., 2013. Characterization and determination of 2-(2-phenylethyl) chromones in agarwood by GC-MS. Molecules, 18(10), 12324-12345.
47. Meng, Y., Pino, V., Anderson, J.L., 2011. Role of counteranions in polymeric ionic liquid-based solid-phase microextraction coatings for the selective extraction of polar compounds. Analytica Chimica Acta, 687(2), 141-149.
48. Mohamed, R., Jong, P.L., Nurul Irdayu, I., 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(9), 2427-2436.
49. Mohamed, R., Jong, P.L., Zali, M.S., 2010. Fungal diversity in wounded stems of Aquilaria malaccensis. Fungal Diversity, 43(1), 67-74.
50. Msaada, K., Hosni, K., Taarit, M.B., Chahed, T., Kchouk, M.E., Marzouk, B., 2007. Changes on essential oil composition of coriander (Coriandrum sativum L.) fruits during three stages of maturity. Food Chemistry, 102(4), 1131-1134.
51. Mulyaningsih, T., 2002. Formation of interxylary phloem and aromatic resin in Gyrinops versteegii (Thymelaeaceae). IAWA Journal, 23(4), 472-473.
52. Ng, L.T., Chang, Y.S., Kadir, A.A., 1997. A review on agar (gaharu) producing Aquilaria species. Journal of Tropical Forest Products, 2(2), 272-285.
53. Nguyen, T.T.T., 2014. Biodiversity of major bacterial groups in association with agarwood (Aquilaria crassna) in Khanh Hoa province, Vietnam. Journal of Vietnamese Environment, 6(2), 132-137.
54. Norhayati, M., Erneeza, M.H., Kamaruzaman, S., 2016. Morphological, pathogenic and molecular characterization of Lasiodiplodia theobromae: A causal pathogen of black rot disease on kenaf seeds in Malaysia. International Journal of Agriculture & Biology, 18(1), 80-85.
55. Novriyanti, E., Santosa, E., 2011. The role of phenolics in agarwood formation of Aquilaria crassna Pierre ex Lecomte AND Aquilaria microcarpa Baill Trees. Indonesian Journal of Forestry Research, 8(2), 101-113.
56. Novriyanti, E., Santosa, E., Syafii, W., Turjaman, M., Sitepu, I.R., 2010. Anti fungal activity of wood extract of Aquilaria crassna Pierre ex Lecomte against agarwood-inducing fungi, Fusarium solani. Indonesian Journal of Forestry Research, 7(2), 155-165.
57. Nurbaya, T.K., Baharuddin, A.R.D.S.M., 2014. Tentative identification of fungal isolates assosiated with Aquillaria spp. from remaining forest areas in Nunukan regency, North Kalimantan.
58. Parveen, Z., Siddique, S., Ali, Z., 2014. Chemical composition of essential oil from leaves of seeded and seedless Citrus reticulata Blanco var. kinnow. Bangladesh Journal of Scientific and Industrial Research, 49(3), 181-184.
59. Pavel, M., Radulescu, V., Ilies, D.C., 2009. GC-MS analysis of essential oil obtained from the species Thymus comosus Heuff. ex Griseb.(Lamiaceae). Farmacia, 57(4), 479-484.
60. PERsOOn, G.A., 2007. Agarwood: the life of a wounded tree.
61. Pinney, J.W., 2011. Host-pathogen systems biology. Handbook of statistical systems biology, 451-466.
62. Premalatha, K., Kalra, A.J.F.E., 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(3), 205-211.
63. Pripdeevech, P., Khummueng, W., Park, S.K., 2011. Identification of odor-active components of agarwood essential oils from Thailand by solid phase microextraction-GC/MS and GC-O. Journal of Essential Oil Research, 23(4), 46-53.
64. Putri, N., Karlinasari, L., Turjaman, M., Wahyudi, I., Nandika, D., 2017. Evaluation of incense-resinous wood formation in agarwood (Aquilaria malaccensis Lam.) using sonic tomography. Agriculture and Natural Resources, 51(2), 84-90.
65. Rahayu, G., 2010. Induction of agarwood formation by combination of acremonium and chemical treatments. http://repository.ipb.ac.id/handle/123456789/58961.
66. Ramli, A.N.M., Yusof, S., Bhuyar, P., Aminan, A.W., Tajuddin, S.N., Hamid, H.A., 2022. Production of Volatile Compounds by a Variety of Fungi in Artificially Inoculated and Naturally Infected Aquilaria malaccensis. Current Microbiology, 79(5), 1-14.
67. Saikia, P., Khan, M.L., 2012. Agar (Aquilaria malaccensis Lam.): a promising crop in the homegardens of Upper Assam, northeastern India. Journal of Tropical Agriculture, 50(1), 8-14.
68. Sangareswari, M., Parthiban, K.T., Kanna, S.U., Karthiba, L., Saravanakumar, D., 2016. Fungal microbes associated with agarwood formation. American Journal of Plant Sciences, 7(10), 1445.
69. Santoso, E., Irianto, R.S.B., Turjaman, M., Sitepu, I.R., 2011. Gaharu-producing tree induction technology. Proceeding of Gaharu Workshop, Development of Gaharu Production Technology, (pp. 31-45).
70. Satdive, R.K., Fulzele, D.P., Eapen, S., 2007. Enhanced production of azadirachtin by hairy root cultures of Azadirachta indica A. Juss by elicitation and media optimization. Journal of Biotechnology, 128(2), 281-289.
71. Sen, S., Dehingia, M., Talukdar, N.C., Khan, M., 2017. Chemometric analysis reveals links in the formation of fragrant bio-molecules during agarwood (Aquilaria malaccensis) and fungal interactions. Scientific Reports, 7(1), 44406.
72. Shahnazi, S., Meon, S., Vadamalai, G., Ahmad, K., Nejat, N., 2012. Morphological and molecular characterization of Fusarium spp. associated with yellowing disease of black pepper (Piper nigrum L.) in Malaysia. Journal of General Plant Pathology, 78(3), 160-169.
73. Sulaiman, R., Thanarajoo, S.S., Kadir, J., Vadamalai, G., 2012. First report of Lasiodiplodia theobromae causing stem canker of Jatropha curcas in Malaysia. Plant Disease, 96(5), 767.
74. Sumadiwangsa, S., 1997. Agarwood as a high-value commodity in East Kalimantan [Kayu gaharu komoditi elit di Kalimantan Timur]. Duta Rimba, 20(205/206), 33-40.
75. Sumarna, Y., 2005. Strategi Budidaya dan Pengembangan Produksi Gaharu. In Prosiding Seminar Nasional Gaharu, Seameo-Biotrop, Bogor (pp. 1-2).
76. Tamuli, P., Baruah, P., Samanta, R., 2011. Enzyme activities of agarwood (Aquilaria malaccensis Lamk.) stem under pathogenesis. Journal of Spices and Aromatic Crops, 17(3), 240-243.
77. Taniguchi, S., Miyoshi, S., Tamaoki, D., Yamada, S., Tanaka, K., Uji, Y., Gomi, K., 2014. Isolation of jasmonate-induced sesquiterpene synthase of rice: product of which has an antifungal activity against Magnaporthe oryzae. Journal of Plant Physiology, 171(8), 625-632.
78. Tarigan, M., Wingfield, M.J., Van Wyk, M., Tjahjono, B., Roux, J., 2011. Pruning quality affects infection of Acacia mangium and A. crassicarpa by Ceratocystis acaciivora and Lasiodiplodia theobromae. Southern Forests: a Journal of Forest Science, 73(3-4), 187-191.
79. Tian, J.J., Gao, X.X., Zhang, W.M., Wang, L., Qu, L.H., 2013. Molecular identification of endophytic fungi from Aquilaria sinensis and artificial agarwood induced by pinholes-infusion technique. African Journal of Biotechnology, 12(21).
80. Tsan, P.L.J.P., Mohamed, R., 2014. Gas chromatography-mass spectrometry analysis of agarwood extracts from mature and juvenile Aquilaria malaccensis. International Journal of Agriculture and Biology, 16(3), 644-648.
81. Vichi, S., Castellote, A.I., Pizzale, L., Conte, L.S., Buxaderas, S., Lopez-Tamames, E., 2003. Analysis of virgin olive oil volatile compounds by headspace solid-phase microextraction coupled to gas chromatography with mass spectrometric and flame ionization detection. Journal of Chromatography A, 983(1-2), 19-33.
82. Wang, S., Nomura, N., Nakajima, T., Uchiyama, H., 2012. Case study of the relationship between fungi and bacteria associated with high-molecular-weight polycyclic aromatic hydrocarbon degradation. Journal of Bioscience and Bioengineering, 113(5), 624-630.
83. Wiriadinata, H., Semiadi, G., Darnaedi, D., Waluyo, E.B., 2010. Konsep Budidaya gaharu (Aquilaria spp.) di Provinsi Bengkulu. Jurnal Penelitian Hutan dan Konservasi Alam, 7(4), 371-380.
84. Wu, B., Lee, J.G., Lim, C.J., Jia, S.D., Kwon, S.W., Hwang, G.S., Park, J.H., 2012. 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(4), 636-642.
85. Zhang, C.L., Zheng, B.Q., Lao, J.P., Mao, L.J., Chen, S.Y., Kubicek, C.P., Lin, F.C., 2008. Clavatol and patulin formation as the antagonistic principle of Aspergillus clavatonanicus, an endophytic fungus of Taxus mairei. Applied Microbiology and Biotechnology, 78(5), 833-840.
86. Zhang, Z., Yang, Y., Meng, H., Sui, C.H., Wei, J.H., Chen, H.Q., 2010. Advances in studies on mechanism of agarwood formation in Aquilaria sinensis and its hypothesis of agarwood formation induced by defense response. Chinese Traditional and Herbal Drugs, 41(1), 156-159.
87. Zhang, Z., Zhang, X., Yang, Y., Wei, J.H., Meng, H., Gao, Z.H., Xu, Y.H., 2014. Hydrogen peroxide induces vessel occlusions and stimulates sesquiterpenes accumulation in stems of Aquilaria sinensis. Plant Growth Regulation, 72(1), 81-87.
88. Zviely, M., Li, M., 2013. Sesquiterpenoids: the holy fragrance ingredients. Perfumer Flavorist, 38, 52-55.