History and perspectives of induction technology for agarwood production from cultivated Aquilaria in Asia: a review

Abstract

Agarwood, the resinous product of Aquilaria spp. (Thymelaeaceae), is highly valued for medicinal and fragrant purposes. Unsustainable forest harvesting contributes to the declining population in the wild, threatening their existence. As a protection effort, cultivation occurred in range countries, mainly in Asia, effectively establishing mass plantations. The success of domesticating Aquilaria relies heavily on technological advancement in agarwood induction, without which the entire thriving industry will collapse. In this paper, we describe efforts since 1929 and current progress and variation in induction as practiced in Asia. The methods include traditional practices and artificial induction via inoculum and chemical inducer, experimented and patented or otherwise. Artificial induction methods are being developed to intensify agarwood production in terms of yield and quality. While traditional methods are commonly applied by rural planters, artificial methods with the use of specific agents/chemicals are seen as more appealing for inducing agarwood, and have a higher demand from entrepreneurs and plantation owners. Several issues related to induction technology faced by stakeholders in agarwood cultivation are presented, such as safety levels, cost, yields, and quality. We conclude by highlighting remaining challenges in induction methods and their associated technologies.

Keywords

Aquilaria / Agarwood / Cultivation / ‘Gaharu’ / Inducer / Inoculum

References

Akhsan N, Mardji D, Sutisna M. Response of Aquilaria microcarpa to two species of Fusarium under two different cultivation systems. J Trop For Sci, 2015, 27: 447-455.

Bhattacharyya B, Datta A, Baruah HK. On the formation and development of agaru in Aquilaria agallocha. Sci Cult, 1952, 18: 240-241.

Biobenua Teknoloji Sdn Bhd (2013) Black Gold Bio Booster (BGBB). http://biobenuagaharu.com.my/?page_id=24. Accessed 12 Dec 2016

Bisnis Gaharu (2015) Inokulan Nanoteknologi Gaharuda. http://bisnisgaharu.com/tag/harga-serum-inokulasi/. Accessed 12 Dec 2016

Blanchette RA, van Beek HH (2005) Cultivated agarwood. U.S. Patent and Trademark Office, Washington, DC, pp 1–15. US Patent 6848211

Bose SR (1943) Agaru production by fungal inoculation in Aquilaria agallocha trees in Assam. In: Proceedings of the 30th Indian Scientific Congress. https://www.cabdirect.org/cabdirect/abstract/19430625104. Accessed 12 Dec 16

Budi S, Santoso E, Wahyudi A. Identification of potential types of fungi on establishment agarwood stem of Aquilaria spp.. Jurnal Silvikultur Tropika, 2010, 1: 1-5.

Chen X, Sui C, Liu Y, Yang Y, Liu P, Zhang Z, Wei J. Agarwood formation induced by fermentation liquid of Lasiodiplodia theobromae, the dominating fungus in wounded wood of Aquilaria sinensis. Curr Microbiol, 2017, 74: 460-468.

Chhipa H, Chowdhary K, Kaushik N. Artificial production of agarwood oil in Aquilaria sp. by fungi: a review. Phytochem Rev, 2017

Chong SP, Osman MF, Bahari N, Nuri EA, Zakaria R, Abdul-Rahim K. Agarwood inducement technology: a method for producing oil grade agarwood in cultivated Aquilaria malaccensis Lamk. J Agrobiotechnol, 2015, 6: 1-16.

Chowdhury M, Hussain MD, Chung SO, Kabir E, Rahman A. Agarwood manufacturing: a multidisciplinary opportunity for economy of Bangladesh—a review. CIGR J, 2016, 18: 171-178.

CITES Secretariat (2004) Convention on international trade in endangered species of Wild Fauna and Flora. CoP13 Prop. 49. Consideration of proposals for amendment of Appendices I and II-Aquilaria spp. and Gyrinops spp. Thirteenth meeting of the conference of the parties, 2–14 Oct 2004, Bangkok. International Environment House, Geneva, pp 1–9

Cui J, Wang C, Guo S, Yang L, Xiao P, Wang M. Evaluation of fungus-induced agilawood from Aquilaria sinensis in China. Symbiosis, 2013, 60: 37-44.

Dinh XB (2015) Vietnamese farmers uses ants to create rare aloeswood. J Glob Issues Solut. http://www.bwwsociety.org/journal/archive/applied_biology.htm. Accessed 26 Dec 2016

Faizal A, Esyanti RR, Aulianisa EN, Santoso E, Turjaman M. Formation of agarwood from Aquilaria malaccensis in response to inoculation of local strains of Fusarium solani. Trees, 2017, 31: 189-197.

Fu J, Xu Y (2016) A natural method of bionic colorectal fragrant incense. CN104082058B. State Intellectual Property office of the P.R.C., Beijing, pp 1–8

Gaharu Anugerah Sarawak (2013) GAS de_Denai agarwood inducer. http://gaharu-anugerah-sarawak.blogspot.my/p/researh-and-development.html. Accessed 13 Jan 2017

Gaharu Sarawak (2015) Inokulan SGB. http://gaharusarawak.blogspot.my/. Accessed 30 Nov 2016

Gibson IAS. The role of fungi in the origin of oleoresin deposits (agaru) in the wood of Aquilaria agallocha Roxb. Bano Biggyan Patrika, 1977, 6: 16-26.

Gunawan H (2012) Gaharu on. http://hergunfish.blogspot.my/2012/07/inokulan-gaharu-on-hergun-pengembang.html. Accessed 13 Jan 2017

Hashim JRN, Mustapa MZ, Othman K (2016) Agarwood: policy and regulations in Malaysia. Paper presented at the 2nd international scientific symposium on agarwood, 10–12 Oct 2016, Putrajaya, Malaysia. Universiti Putra Malaysia, Serdang, p 12

Hawksworth DL, Gibson IAS. Phialophora parasitica. C.M.I. Descriptions of pathogenic fungi and bacteria, 1976, Kew: Commonwealth Mycological Institute 504

Huang Z (2013) Method for producing high-quality Aquilaria sinensis material through Aspergillus niger conversion. CN103215311A. State Intellectual Property office of the P.R.C., Beijing, pp 1–12

Huang J, Liao Y, Chen H, Zhang Z. Chemical solution is an efficient method to induce the formation of 2-(2-phenylethyl) chromone derivatives in Aquilaria sinensis. Phytochem Lett, 2017, 19: 64-70.

Iskandar D, Suhendra A. Uji inokulasi Fusarium sp. untuk produksi gaharu pada budidaya A. beccariana. Jurnal Sains dan Teknologi Indonesia, 2012, 14: 182-188.

Ismail N, Nor Azah MA, Jamil M, Rahiman MH, Tajuddin SN, Taib MN. Analysis of high quality agarwood oil chemical compounds by means of SPME/GC-MS and Z-score technique. Malays J Anal Sci, 2013, 17: 403-413.

Ismail N, Ali NAM, Jamil M, Rahiman MH, Tajuddin SN, Taib MN. A review study of agarwood oils and its quality analysis. Jurnal Teknologi (Sci Eng), 2014, 68: 37-42.

ITTO-CITES (2015) Report of the Asian regional workshop on management of wild and planted agarwood taxa, 19–23 Jan 2015. Guwahati, Assam, India. International Timber Trade Organization (ITTO), Yokohama, pp 1–17

IUCN (2017) The IUCN red list of threatened species. Version 2017-1. http://www.iucnredlist.org. Accessed 12 Dec 2016

Jailani AK (2015). Inokulan Gaharu Bio Inducer. http://gaharu84.blogspot.my/2015/11/harga-gubal-gaharu-budidaya-dan.html. Accessed 20 Dec 2016

Jalaluddin M. A useful pathological condition of wood. Econ Bot, 1977, 31: 222-224.

Jamil M, Ali NAM, Saidin SH, Lias S, Zainal MH, Aziz A, Patah MFZ. Jamal JA, Ali MS, Jalil J, Husain K, Azmi N, Jasamai M, Kumulosasi E. Volatile components, extractive content and E-Nose study on two natural B grade agarwood samples. Proceeding of the 30th annual seminar of the Malaysian Natural Products Society, 18–19 Mar 2014, Bangi, Selangor, 2014, Bangi: Universiti Kebangsaan Malaysia 93 96

Jayaraman S, Mohamed R. Crude extract of Trichoderma elicits agarwood substances in cell suspension culture of the tropical tree, Aquilaria malaccensis Lam. Turk J Agric For, 2015, 39: 163-173.

Jong PL, Tsan P, Mohamed R. Gas chromatography-mass spectrometry analysis of agarwood extracts from mature and juvenile Aquilaria malaccensis. Int J Agric Biol, 2014, 16: 644-648.

Lan J, Li H (2013) Method for producing agilawood on Aquilaria plant by eccentric perfusion method. CN102668908A. State Intellectual Property office of the P.R.C., Beijing, pp 1–10

Lee SY, Mohamed R. Mohamed R. The origin and domestication of Aquilaria, an important agarwood-producing genus. Agarwood: science behind the fragrance, 2016, Singapore: Springer 1 20

Li W, Cai C, Dong W, Guo Z, Wang H, Mei W, Dai H. 2-(2-Phenylethyl) chromone derivatives from Chinese agarwood induced by artificial holing. Fitoterapia, 2014, 98: 117-123.

Lin F, Mei W, Wu J, Dai H. GC-MS analysis of volatile constituents from Chinese eaglewood produced by artificial methods. Zhong Yao Cai, 2010, 33: 222-225.

Lisdayani L, Anna N, Siregar EBM. Isolation and identifying of fungi from the stem of agarwood (Aquilaria malaccensis Lamk.) was had been inoculation. Peronema For Sci J, 2015, 4: 1-5.

Liu Y, Chen H, Yang Y, Zhang Z, Wei J, Meng H, Gao Z. Whole-tree agarwood-inducing technique: an efficient novel technique for producing high-quality agarwood in cultivated Aquilaria sinensis trees. Molecules, 2013, 18: 3086-3106.

Liu Y, Wei J, Gao Z, Zhang Z, Lyu J. A review of quality assessment and grading for agarwood. Chin Herb Med, 2017, 9: 22-30.

Ma H, Liang K, Zhou Z, Huang G, Lin M (2012) Method for rapid formation of agilawood of agallochum through induction by using fungus fermentation liquid. CN102550311A. State Intellectual Property office of the P.R.C., Beijing, pp 1–6

Marapurna A (2016) Bio Serum Gaharu Lampung. http://bioserumgaharulampung.blogspot.my/. Accessed 26 Dec 2016

Martin D, Tholl D, Gershenzon J, Bohlmann J. Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol, 2002, 129: 1003-1018.

Mei W, Dai H, Wang H, Cai Z (2014) Agilawood production method. CN103229677A. State Intellectual Property office of the P.R.C., Beijing, pp 1–8

Mohamed R, Lee SY. Mohamed R. Keeping up appearances: agarwood grades and quality. Agarwood: science behind the fragrance, 2016, Singapore: Springer 149 167

Mohamed R, Jong PL, Zali MS. Fungal diversity in wounded stems of Aquilaria malaccensis. Fungal Divers, 2010, 43: 67-74.

Mohamed R, Wong MT, Halis R. Microscopic observation of ‘gaharu’ wood from Aquilaria malaccensis. Pertanika J Sci Technol, 2013, 36: 43-50.

Mohamed R, Jong PL, Kamziah AK. Fungal inoculation induces agarwood in young Aquilaria malaccensis trees in the nursery. J For Res, 2014, 25: 201-204.

Monggoot S, Popluechai S, Gentekaki E, Pripdeevech P. Fungal endophytes: an alternative source for production of volatile compounds from agarwood oil of Aquilaria subintegra. Microb Ecol, 2017

Naef R. The volatile and semi-volatile constituents of agarwood, the infected heartwood of Aquilaria species: a review. Flavour Frag J, 2011, 26: 73-87.

Ng LT, Chang YS, Azizol AK. A review on agar (gaharu) producing Aquilaria species. J Trop For Prod, 1997, 2: 272-285.

Nobuchi T, Sahri MH. The formation of wood in tropical forest trees: a challenge from the perspective of functional wood anatomy, 2008, Serdang: Penerbit Universiti Putra Malaysia.

Okudera Y, Ito M. Production of agarwood fragrant constituents in Aquilaria calli and cell suspension cultures. Plant Biotechnol, 2009, 26: 307-315.

Phillips MA, Walter MH, Ralph SG, Dabrowska P, Luck K, Uros EM. Functional identification and differential expression of 1-deoxy-D-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol Biol, 2007, 65: 243-257.

Pojanagaroon SC, Kaewrak C. Mechanical methods to stimulate aloes wood formation in Aquilaria crassna Pierre ex H. Lec. (kritsana) trees. Acta Hortic, 2005, 676: 161-166.

Rahman MA, Basak AC. Agar production in agar trees by artificial inoculation and wounding. Bano Biggyan Patrika, 1980, 9: 87-93.

Rahman MA, Khisa SK. Agar production in agar tree by artificial inoculation and wounding, part-II, further evidences in favor of agar formation. Bono Biggyan Patrika, 1984, 9: 57-63.

Rasool S, Mohamed R. Mohamed R. Understanding agarwood formation and its challenges. Agarwood: science behind the fragrance, 2016, Singapore: Springer 39 56

Rusli J (2011) Inokulan Gaharu Biotech (IGB) and Nano Tech. http://gaharucandanku.blogspot.my/search/label/Inokulan%20Gaharu%20Biotech. Accessed 20 Dec 2016

Sadgopal VB. Exploratory studies in the development of essential oils and their constituents in aromatic plants. Part I. Oil of agarwood. Soap Perfum Cosmet (Lond), 1960, 33: 41-46.

Santoso E. Turjaman M. Pembentukan gaharu dengan cara inokulasi. Makalah diskusi hasil penelitian dalam menunjang pemanfaatan hutan yang lestari, 11–12 Mar 1996, Bogor, 1996, Bogor: Pusat Litbang Hutan dan Konservasi Alam 1 3

Santoso E, Irianto RSB, Turjaman M, Sitepu IR, Santoso S, Najmulah, Yani A, Aryanto. Turjaman M. Gaharu-producing tree induction technology. Proceedings of the development of gaharu production technology, 1 July 2011, 2011, Bogor: Research and Development Centre for Forest Conservation and Rehabilitation 31 46

Sripetkla W (2011) Witsawa’s Agarwood Inducer. http://agarwoodinducement.blogspot.my/. Accessed 08 Jan 2017

Tabata Y, Widjaja E, Mulyaningsih T, Parman I, Wiriadinata H, Mandang YI, Itoh T. Structural survey and artificial induction of aloeswood. Wood Res : Bull Wood Res Inst Kyoto Univ, 2003, 90: 11-12.

Tamuli P, Boruah P, Nath SC, Samanta R. Fungi from diseased agarwood tree (Aquilaria agallocha Roxb.): two new records. Adv For Res India, 2000, 22: 182-187.

Tamuli P, Boruah P, Nath SC, Leclercq P. Essential oil of eaglewood tree: a product of pathogenesis. J Essent Oil Res, 2005, 17: 601-604.

Tanali Esteem (2013) Gaharu Resin Essence. http://www.tanali.my/Gaharu-Essence.html. Accessed 05 Jan 2017

Tang W (2016) Method for generating fragrance of agilawood through natural fungi. CN105830765A. State Intellectual Property office of the P.R.C., Beijing, pp 1–6

Tang J, Liu Y (2016) A natural incense inducer and methods of producing agarwood. CN103858689A. State Intellectual Property office of the P.R.C., Beijing, pp 1–5

Telupid Gaharu Enterprise (2009) Vaksin NVI, PLT (Gred A, B, and C), and Vaksin Kuning. http://telupidgaharu.blogspot.my/. Accessed 12 Dec 16

Thanh L, Do T, Son NH, Sato T, Kozan O. Impacts of biological, chemical and mechanical treatments on sesquiterpene content in stems of planted Aquilaria crassna trees. Agrofor Syst, 2015, 6: 973-981.

The Plant List (2013) Version 1.1. Published on the Internet. http://www.theplantlist.org/. Accessed 12 Dec 2016

Tian J, Gao X, Zhang W, Wang L, Qu L. Molecular identification of endophytic fungi from Aquilaria sinensis and artificial agarwood induced by pinholes-infusion technique. Afr J Biotechnol, 2013, 12: 3115-3131.

Triadiati T, Carolina DA, Miftahudin. Induksi pembentukan gaharu menggunakan berbagai media tanam dan cendawan Acremonium sp. dan Fusarium sp. pada Aquilaria crassna. Jurnal Sumberdaya Hayati, 2016, 2: 1-6.

Turjaman M, Hidayat A. Agarwood-planted tree inventory in Indonesia. IOP Conf Ser Earth Environ Sci, 2017, 54: 012062.

UNEP-WCMC (Comps) (2015) The checklist of CITES species website. CITES Secretariat, Geneva, Switzerland. Compiled by UNEP-WCMC, Cambridge, UK. http://checklist.cites.org. Accessed 17 Jan 2017

Verma VPS. Trials of herbicides for inducing formation of agarwood in Aquilaria agollocha Roxb. Indian Perfum, 1977, 21: 151-153.

Wei J, Yang Y, Zhang Z, Meng M, Feng J, Gan B (2010) Liquid infusion method for producing linaloe on Aquilaria sinensis tree. CN101755629. State Intellectual Property office of the P.R.C., Beijing, pp 1–5

Wei J, Chen X, Yang Y, Liu Y, Zhang Z, Su Z (2014) Fungus for promoting Aquilaria plants to generate agilawood and application of fungus. CN103651151A. State Intellectual Property office of the P.R.C., Beijing, pp 1–8

Wei J, Chen X, Yang Y, Liu Y, Meng H, Zhang Z, Gan B (2016) Microorganism liquid infusion method-based agilawood induction method and application. CN105340601A. State Intellectual Property office of the P.R.C., Beijing, pp 1–12

Wijitphan P (2009) Method to stimulate resin formation by wounding on the Aquilaria’s trunk. Patent and Trademark Office, Washington, DC, pp 1–11. US Patent 7485309

Wyn LT, Anak NA. Wood for the trees: a review of the agarwood (gaharu) trade in, 2010, Selangor: TRAFFIC Southeast Asia.

Yan H, Lin C (2016) Method for resin secretion process of agilawood. CN105409715A. State Intellectual Property office of the P.R.C., Beijing, pp 1–8

Yang M, Fu H, Liang Y, Huang H, Zhao B, Xie C, Chen N. Modified transfusion devices, inducer, and procedure for agarwood-inducing by infusion technique. J Chem Pharm Res, 2014, 6: 2566-2571.

Yazid A, Al-Fattah SS (2017) PIT2008. http://wafiqahfarmnursery.blogspot.my/. Accessed 12 Dec 2016

Yin Y, Jiao L, Dong M, Jiang X, Zhang S. Mohamed R. Wood resources, identification, and utilization of agarwood in China. agarwood, 2016, Singapore: Springer 21 38

Zeneli G, Krokene P, Christiansen E, Krekling T, Gershenzon J. Methyl jasmonate treatment of mature Norway spruce (Picea abies) trees increases the accumulation of terpenoid resin components and protects against infection by Ceratocystis polonica, a bark beetle-associated fungus. Tree Physiol, 2006, 26: 977-988.

Zhang X, Liu Y, Wei J, Yang Y, Zhang Z, Huang J, Liu Y. Production of high-quality agarwood in Aquilaria sinensis trees via whole-tree agarwood-induction technology. Chin Chem Lett, 2012, 23: 727-730.

Zhang Z, Han X, Wei J, Xue J, Yang Y, Liang L, Gao Z. Compositions and antifungal activities of essential oils from agarwood of Aquilaria sinensis (Lour.) Gilg induced by Lasiodiplodia theobromae (Pat.) Griffon. and Maubl. J Braz Chem Soc, 2014, 25: 20-26.