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Diversity and Biosynthetic Activities of Agarwood Associated Fungi

Tian-Ye Du
Cheng-Jiao Dao
Ausana Mapook
Steven L. Stephenson
Abdallah M. Elgorban
Salim Al-Rejaie
Nakarin Suwannarach
Samantha C. Karunarathna
1,* and
Saowaluck Tibpromma
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing 655011, China
Centre of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
College of Resources and Environment, Yunnan Agricultural University, 452 Fengyuan Road, Kunming 650201, China
Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USA
Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
Department of Pharmacology & Toxicology, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
Research Center of Microbial Diversity and Sustainable Utilization, Chiang Mai University, Chiang Mai 50200, Thailand
Authors to whom correspondence should be addressed.
Diversity 2022, 14(3), 211;
Submission received: 14 February 2022 / Revised: 4 March 2022 / Accepted: 8 March 2022 / Published: 11 March 2022
(This article belongs to the Topic Fungal Diversity)


Agarwood is a fragrant dark resin produced in plants belonging to the family Thyme-laeaceae and which has a high economic value. The unique fragrance and medicinal applications intensify the value of agarwood. The wild populations of agarwood trees are highly threatened by high economic demand. Therefore, it is worthwhile to develop an artificial agarwood induction technology for the countries that rely on agarwood from the natural habitat of the plants. Fungal induction of agarwood has been shown to be an efficient method. Interestingly, most of the fungi known from agarwood are endophytic. In this paper, we supplement and update the bioactivity of fungi associated with agarwood and their ability to induce agarwood formation. According to the existing literature, 59 endophytic fungal strains of 16 genera induce agarwood production, most of which belong to Fusarium (28 identified strains). Hence, Fusarium is a good candidate for further studies on fungal induced agarwood production.

1. Introduction

Agarwood is a highly valuable, fragrant, and dark resinous heartwood of trees in the family Thymelaeaceae [1,2,3,4]. Agarwood is also known under different names in different regions, including agar (Hindi), akil (Tamil), aloe wood (Indonesian), chen xiang (Chinese), chim-hyuang (Korean), eaglewood (Papua New Guinea), gaharu (Malaysian), jin-koh (Japanese), mai ketsana (Lao), mai kritsana (Thai), oud (Arabic), oud or agar attar (Middle Eastern), sasi or sashi (Assamese), and tramhuong (Vietnamese) [5,6,7]. The plants in the family Thymelaeaceae, especially the genera Aquilaria and Gyrinops, are well known for agarwood production, and these are grown in several countries in Southeast Asia (e.g., Borneo, Cambodia, China, India, Indonesia, Laos, Malaysia, New Guinea, Thailand, Philippines, and Vietnam) [2,3,8,9]. Agarwood has been referred to as the “woods of the Gods”, and it has been widely used as incense, perfumes (essential oils), in medicine and religious ceremonies [2,10,11,12,13,14,15].
The price of agarwood varies with the quality of its resin [7,16]. The best agarwood ranges from $100,000 to 800,000 per kilogram, while the price of other agarwood ranges from $500 to 100,000 per kilogram according to the grade. The essential oil of agarwood in the global market is sold for $30,000 per liter (, accessed on 9 March 2022). In the past decade, agarwood reached its highest commercial demand when the demand exceeded the supply mainly due to the fact that good quality agarwood is formed slowly and infrequently in old trees and the increase in consumers [17,18,19,20]. High economic value and high demand lead to overexploitation of the wild mother trees [21]. This affects mature populations of the plants and puts the future of the industry at great risk [21]. All species of Aquilaria and Gyrinops have been presented in Appendix II based on the data available at “Convention on International Trade in Endangered Species (CITES) in 2005” [6,21,22,23].
Under natural conditions, the formation of agarwood is rare and very slow [24,25]. Agarwood is produced when healthy white wood is damaged (lightning strike, strong wind, animal grazing and insect attack) and infected with microorganisms [7,24]. The infection stimulates the plant defense response; as a result, the dark resin is produced to suppress further infection [24,26].
For the sustainable development of the agarwood industry, many agarwood-producing countries (Cambodia, China, Indonesia, Malaysia, Thailand, and Vietnam) have been committed to developing artificial induction of agarwood resin in agarwood tree plantations [6,9]. The three common induction techniques are physical, chemical, and biological [7,9]. Among these three factors, biological (fungal inoculation) is considered to be effective, and most of the fungi used for inoculation are endophytes isolated from healthy or diseased wood of agarwood-producing trees [9,27,28]. Therefore, many scientists have been committed to isolating various endophytic fungi from different parts of agarwood-producing trees and confirming that some endophytic fungi such as Aspergillus niger [28], Fusarium solani [26], Lasiodiplodia theobromae [29], and Melanotus flavolivens [30] induce agarwood production. Moreover, the endophytic fungi associated with agarwood-producing trees contain biologically active components (e.g., Diaporthe sp.—antioxidant capacity [31]; Nemania aquilariae—antibacterial and antimicrobial properties [25]; Xylaria mali—antimicrobial and antitumor activity [32]).
In this paper, we review the biological activity and agarwood induction potential of endophytic fungi isolated from agarwood plants. Furthermore, we provide references for better research on the sustainable development of agarwood production through novel technologies.

1.1. Agarwood-Producing Trees and Their Geographical Distribution

Agarwood is produced in trees belonging to the family Thymelaeaceae (Aetoxylon, Aquilaria, Gonystylus and Gyrinops) [33]. Among the species in the Thymelaeaceae, Aquilaria and Gyrinops are well-known for agarwood production [21]. Aquilaria and Gyrinops belong to the same subfamily Thymelaeoideae (previously Aquilariodeae), and the two species are very similar in morphology [33]. However, the flowers in Aquilaria have eight to twelve stamens, while those in Gyrinops have five stamens [33].
Agarwood-producing trees are evergreen broadleaf trees that occur in the tropics [6,8]. They are native to Southeast Asia and are mostly distributed in the rainforests of Borneo, Cambodia, China, India, Indonesia, Laos, Malaysia, New Guinea, Philippines, Thailand, and Vietnam [2,3]. However, Indonesia has the highest diversity of natural agarwood plant species [21]. Agarwood plantations in Indonesia are relatively small (10 to 5000 trees per farmer), while in Cambodia, China, Laos, Malaysia, Thailand, and Vietnam, the plantation area is larger, ranging from 40 hectares to more than 1000 hectares [21].

1.2. Fragrant Purposes and Medicinal Uses of Agarwood

Agarwood is well known as incense because it has a pleasant fragrance when it is burned [11,14]. However, the essential oil of agarwood is the most important ingredient in high-end perfume due to its unique fragrance [11,14]. Agarwood has been widely used in Buddhist, Hindu, and Islamic ceremonies [2]. In the Middle East, agarwood is a famous incense, and the essential oil is being used as high demanding perfumes [18,34]. In addition, agarwood incense plays an important role in the Japanese “koh-doh” ceremony [19,34].
Agarwood plays an important role in both traditional and modern medicine [2,12,13]. In traditional Chinese medicine, agarwood is used as a sedative, qi-regulating drug, and carminative medicine, which can also alleviate stomach disease, cough, rheumatism, and high fever [2,12,13]. In traditional Indian medicine, agarwood is used to treat diarrhea, dysentery, vomiting, anorexia, oral and dental diseases, facial paralysis, tremor, sprain, and fracture [34,35]. In traditional Arabian medicine, agarwood essential oil is often used in aromatherapy [2]. Modern pharmacological research has shown that agarwood has the potential of inducing sedation, reducing nerve excitability as well as being antibacterial and antifungal, anti-inflammatory, having analgesic effects, gastrointestinal regulatory properties, antiasthma, anti-diabetes, and antioxidation [2,36].

1.3. Three Methods That Induce the Production of Agarwood

Agarwood is known as the most expensive natural product on the earth, but the formation of its resin is very rare and slow under natural conditions [7,16,24]. In order to meet the needs of the market, long ago, people began to explore the artificial induction methods of agarwood [20,37]. The current artificial induction methods can be summarized in the following three methods (Figure 1).

1.3.1. Physical Injury

The artificial induction technology of agarwood can be traced back to AD 300 in China [20]. Based on the literature, the color of internal tissues (branches, joints, root and stem) changed due to the formation of the resin after one year of artificial injury [20,39]. Farmers used methods such as burning, burning with a red-hot iron, cutting, drilling, holing, nailing the trees, partial pruning tree trunks, peeling and wounding trees with axes or machetes [6,9,12].
The advantage of these physical injury methods is that they are cost-effective, while the disadvantage is that it takes manpower, a few years or even one decade, and the yield is related to the number and degree of physical injury [9].

1.3.2. Chemical Inducer

Different chemicals such as brown sugar, formic acid, hydrogen peroxide, methyl jasmonate, salicylic acid, sodium chloride and soybean oil have been used to stimulate the formation of agarwood [40,41,42,43]. These chemicals are injected into the xylem of the trees in different concentrations and, as a result of being distributed throughout the plant through xylem transportation, cause damages to the whole plant [7].
The advantage of chemical induction is that it is faster, results in higher production, and furthermore, induces the whole plant to form agarwood resin [9,44]. However, the disadvantage of chemical induction is the harmful side effects of the chemicals on the environment [44].

1.3.3. Biological Inoculation (Fungal Inoculation)

The fungal inoculation of an agarwood-producing tree (Aquilaria agallocha) was first reported by Tunstall in 1929 [37]. Later, several studies were carried out to investigate and isolate various fungi from agarwood to induce agarwood production [26,45,46]. Such research confirmed the positive role of fungi in inducing agarwood formation [26,45,46]. At the beginning of the 21st century, there was an immense expansion of research on the role of agarwood tree endophytes on the production of agarwood (Table 1), while some fungi with inducing ability and biological activity have been studied [24,26,32,46,47,48,49,50,51,52,53,54,55,56].
Biological induction techniques involve the stimulation of the plant’s immune response through artificial infection of “pure” or “mixed” fungal strains [9]. The majority of fungi used for the inoculation are endophytes isolated from healthy plants or the infected tissue of agarwood-producing trees [9]. The inoculation is done through open wounds [6]. The long incubation period allows microorganisms to reproduce and settle in the tree [6]. This triggers the plant defense mechanism to produce the agarwood to resist further fungal infections [6,9].
The advantage of biological agarwood induction is that it can intermittently and continuously induce the formation of agarwood [7,57]. Compared with the physical methods, biological agents are faster and more efficient, while compared to chemical methods, they are safer, healthier, and environmentally friendly [21]. In this review, we summarized the data on endophytic fungi isolated from agarwood-producing trees derived from 49 peer-reviewed publications (Table 1). Based on the literature, 171 endophytic strains in 59 genera have been isolated from agarwood plants (Figure 2, Table 1). Among these, 59 endophytic strains in 16 genera have been shown to induce agarwood production through artificial induction experiments (Table 2). In addition, 38 endophytic strains in 29 genera have been evaluated for their biological activities (such as antimicrobial, antimicrobial and antitumor) (Table 3).
Table 1. Endophytic fungi isolated from agarwood-producing trees. “Y” indicates an ability of this strain to induce the formation of agarwood resin, “N” indicates that this strain has not been tested to induce the formation of agarwood resin in the given study; “N/A” indicates that no information available (The table is arranged according to the time of publication).
Table 1. Endophytic fungi isolated from agarwood-producing trees. “Y” indicates an ability of this strain to induce the formation of agarwood resin, “N” indicates that this strain has not been tested to induce the formation of agarwood resin in the given study; “N/A” indicates that no information available (The table is arranged according to the time of publication).
Endophytic FungiAgarwood-Producing Tree SpeciesIsolation SourceThe Ability to Induce AgarwoodBioactivity/Important MetabolitesCountryReferences
Aspergillus sp.Aquilaria sp.N/AYN/AIndia[58]
BotryodyplodisAquilaria sp.N/AYN/AIndia[58]
Botryosphaeria dothideaAquilaria sp.N/AYN/AIndia[58]
Diplodia sp.Aquilaria sp.N/AYN/AIndia[58]
Several fungi isolated from Aquilaria agallochaAquilaria agallochaN/ANN/AN/A[59]
Epicoccum granulatumAquilaria agallochaN/AYN/AIndia[60]
Cladosporium sp.Aquilaria agallochaN/AYN/AN/A[61]
Torula sp.Aquilaria agallochaN/AYN/AN/A[61]
Phialophora parasiticaAquilaria agallochaN/ANN/AN/A[62]
Aspergillus sp.Aquilaria agallochainfected woodNN/AN/A[37]
Aspergillus tamariiAquilaria agallochainfected woodNN/AN/A[37]
Botryodiplodia theobromaeAquilaria agallochainfected woodNN/AN/A[37]
Fusarium solaniAquilaria agallochainfected woodNN/AN/A[37]
Penicillium citrinumAquilaria agallochainfected woodNN/AN/A[37]
Fusarium bulbigeniumAquilaria sp.N/AYN/AN/A[63]
Fusarium lateritiumAquilaria sp.N/AYN/AN/A[63]
Fusarium oxysporumAquilaria sp.N/AYN/AN/A[63]
Melanotus flavolivensAquilaria sinensisN/AYN/AChina[30]
Chaetomium globosumAquilaria agallochaN/AYN/AIndia[47]
Fusarium oxysporumAquilaria agallochaN/AYN/AIndia[47]
Fusarium sp.Aquilaria sp.Agarwood samplesYN/AIndonesia[48]
Fusarium sp.Aquilaria sp.N/AYN/ASumatra island[48]
Fusarium sp.Gyrinops versteegiiAgarwood samplesYN/AIndonesia[48]
Chaetomium globosumAquilaria agallochaN/AYN/AN/A[49]
Fusarium oxysporumAquilaria agallochaN/AYN/AN/A[49]
Acremonium sp.Aquilaria microcarpaN/AYN/AMalaysia[50]
Botryosphaeria rhodinaAquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Cephalosporium sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Cladophialophora sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Cladosporium edgeworthraeAquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Colletotrichum sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Epicoccum sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Fusarium oxysporumAquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Fusarium sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Geotrichum sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Glomerularia sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Gonytrichum sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Guignardia manqiferaeAquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Monilia sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Mortierella sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Mycelia sterilia sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Ovulariopsis sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Penicillium sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Pleospora sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Rhinocladiella sp.Aquilaria sinensisStem, root and leavesNAntimicrobial activityChina[64]
Fusarium moniliformeAquilaria sp.N/AYN/AN/A[51]
Fusarium sambucinumAquilaria sp.N/AYN/AN/A[51]
Fusarium solaniAquilaria sp.N/AYN/AN/A[51]
Fusarium tricinctumAquilaria sp.N/AYN/AN/A[51]
Melanotus flavolivensAquilaria sinensisN/AYSesquiterpenes, aromatic constituents, and fatty acidsChina[65]
Fusarium solaniAquilaria malaccensisWood chipsNN/AMalaysia[66]
Fusarium sp.Aquilaria malaccensisWood chipsNN/AMalaysia[66]
Hypocrea lixiiAquilaria malaccensisWood chipsNN/AMalaysia[66]
Lasiodiplodia theobromaeAquilaria malaccensisWood chipsNN/AMalaysia[66]
Cochliobolus lunatusAquilaria malaccensisWood chipsNN/AMalaysia[66]
Cunninghamella bainieriAquilaria malaccensisWood chipsNN/AMalaysia[66]
Curvularia sp.Aquilaria malaccensisWood chipsNN/AMalaysia[66]
Trichoderma sp.Aquilaria malaccensisWood chipsNN/AMalaysia[66]
Nodulisporium sp.Aquilaria sinensisStemNIsofuranonaphthalenone, and benzopyranChina[67]
Cladosporium tenuissimumAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Coniothyrium nitidaeAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Epicoccum nigrumAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Fusarium equisetiAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Fusarium oxysporumAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Fusarium solaniAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Hypocrea lixiiAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Lasiodiplodia theobromaeAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Leptosphaerulina chartarumAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Paraconiothyrium variabileAquilaria sinensiAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Phaeoacremonium rubrigenumAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Phoma herbarumAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Rhizomucor variabilisAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[68]
Fusarium sp.Aquilaria microcarpaN/AYN/AN/A[52]
Fimetariella rabenhorstiiAquilaria sinensisN/ANFrabenol (Sesquiterpene alcohol)China[69]
Fusarium sp.Aquilaria beccarianaN/AYN/AN/A[53]
Trichoderma spiraleAquilaria sinensisN/ANTrichodermic acid A, trichodermic acid B, known trichodermic acid and trichodermamide AChina[70]
Lasiodiplodia sp.Aquilaria sinensisNatural agarwoodYN/AChina[45]
Xylaria sp.Aquilaria sinensisNatural agarwoodYN/AChina[45]
Paraconiothyrium variabileAquilaria sinensisAgarwood samplesYN/AChina[71]
Alternaria sp.Aquilaria malaccensisWood samplesNN/AIndia[72]
Cladosporium cladosporoidesAquilaria malaccensisWood samplesNN/AIndia[72]
Cladosporium sp.Aquilaria malaccensisWood samplesNN/AIndia[72]
Curvularia sp.Aquilaria malaccensisWood samplesNN/AIndia[72]
Davidiella tassianaAquilaria malaccensisWood samplesNN/AIndia[72]
Fusarium solaniAquilaria malaccensisAgarwood samplesNN/AIndia[72]
Hypocrea fairnosaAquilaria malaccensisWood samplesNN/AIndia[72]
Massarina albocarnisAquilaria malaccensisWood samplesNN/AIndia[72]
PhaeoacremoniumAquilaria malaccensisWood samplesNN/AIndia[72]
Pichia sp.Aquilaria malaccensisWood samplesNN/AIndia[72]
Trichoderma sp.Aquilaria malaccensisWood samplesNN/AIndia[72]
Alternaria sp.Aquilaria sinensis (nonresinous trees)LeavesNN/AChina[32]
Botryosphaeria sp.Aquilaria sinensis (agarwood-producing wounded tree)LeavesYSesquiterpenes, 2-(2-phenylethyl) chromanone, aromatics, fatty acids and estersChina[32]
Chaetomium sp.Aquilaria sinensis (agarwood-producing wounded tree)N/ANN/AChina[32]
Colletotrichum gleosporiodesAquilaria sinensis (agarwood-producing wounded tree)LeavesNN/AChina[32]
Cylindrocladium sp.Aquilaria sinensis (agarwood-producing wounded tree)LeavesNN/AChina[32]
Fusarium sp.Aquilaria sinensis (agarwood-producing wounded tree)N/AYSesquiterpenes, 2-(2-phenylethyl) chromanone, aromatics, fatty acids and estersChina[32]
Mycosphaerella sp.Aquilaria sinensis (nonresinous trees)LeavesNSesquiterpenes, 2-(2-phenylethyl) chromanone, aromatics, fatty acids and estersChina[32]
Nodulisporium sp.Aquilaria sinensis (agarwood-producing wounded tree)N/ANN/AChina[32]
Penicillium sp.Aquilaria sinensis (agarwood-producing wounded tree)N/ANN/AChina[32]
Pestalotiopsis sp.Aquilaria sinensis (agarwood-producing wounded tree)N/ANN/AChina[32]
Phoma sp.Aquilaria sinensis (nonresinous trees)LeavesNN/AChina[32]
Phomopsis sp.Aquilaria sinensis (agarwood-producing wounded tree)LeavesNN/AChina[32]
Ramichloridium sp.Aquilaria sinensis (nonresinous trees)LeavesNN/AChina[32]
Sagenomella sp.Aquilaria sinensis (nonresinous trees)LeavesNN/AChina[32]
Xylaria maliAquilaria sinensisAgarwood samplesNAntimicrobial and antitumor activityChina[32]
Xylaria sp.Aquilaria sinensis (agarwood-producing wounded tree)N/ANN/AChina[32]
Lasiodiplodia theobromaeAquilaria sinensisDiseased branchYJasmonates, JAsChina[29]
Nigrospora oryzaeAquilaria sinensisStem, root and leavesN11-Hydroxycapitulatin B and Capitulatin BChina[73]
Unidentified five fungi belonging to the Deuteromycetes and Ascomycetes Aquilaria malaccensisN/AYBenzylacetone, anisylacetone, guaiene and palustrolMalaysia[54]
Fusarium oxysporumAquilaria sinensisAgarwood samplesYSesquiterpenes (agarospirol), aromatics compounds and alkanesChina[74]
Lasiodiplodia theobromaeAquilaria sinensisAgarwood samplesYSesquiterpenes (agarospirol), aromatics compounds and alkanesChina[74]
Acremonium sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumNN/AN/A[55]
Alternaria sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumNN/AN/A[55]
Cladosporium sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumNN/AN/A[55]
Fusarium sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumYN/AN/A[55]
Mucor sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumNN/AN/A[55]
Nigrospora sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumNN/AN/A[55]
Scopulariopsis sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumNN/AN/A[55]
Scytalidium sp.Aquilaria malaccensisAgarwood samples pre-inoculated with FusariumNN/AN/A[55]
Fusarium oxysporumAquilaria sp.Agarwood samplesNN/AIndonesia[75]
Fusarium solaniAquilaria sp.Agarwood samplesNN/AIndonesia[75]
Fusarium sp.Aquilaria sp.Agarwood samplesNN/AIndonesia[75]
Fusarium verticillioidesAquilaria crassnaAgarwood samplesNAntimicrobial activityVietnam[76]
Geotrichum candiumAquilaria crassnaAgarwood samplesNAntimicrobial activityVietnam[76]
Acremonium sp.Aquilaria crassnaN/AYN/AN/A[56]
Fusarium sp.Aquilaria crassnaN/AYN/AN/A[56]
Fusarium solaniAquilaria sinensisAgarwood samplesYN/AChina[24]
Lasiodiplodia theobromaeAquilaria sinensisAgarwood samplesYN/AChina[24]
Fusarium solaniAquilaria malaccensisFrom wild Aquilaria malaccensisYTridecanoic acid, a-santalol, and spathulenolIndonesia[44]
Fusarium sp.Aquilaria sinensisAgarwood samplesYN/AChina[77]
Lasiodiplodia theobromaeAquilaria sinensis YN/AChina[77]
Arthrinium sp.Aquilaria subintegraFresh heartwood stemsNβ-agarofuran, α-agarofuran, δ-eudesmol, oxo-agarospirol, and β-dihydro agarofuranThailand[31]
Colletotrichum sp.Aquilaria subintegraFresh heartwood stemsNβ-agarofuran, α-agarofuran, δ-eudesmol, oxo-agarospirol, and β-dihydro agarofuranThailand[31]
Diaporthe sp.Aquilaria subintegraFresh heartwood stemsNExcellent antioxidant capacityThailand[31]
Fusarium sp.Aquilaria malaccensisAgarwood samplesYN/AIndia[78]
Rigidoporus vinctusAquilaria sinensisAgarwood samplesYN/AChina[46]
Fusarium oxysporumAquilaria sinensisN/AYN/AChina[79]
Lasiodiplodia theobromaeAquilaria sinensisN/AYN/AChina[79]
Nigrospora oryzaeAquilaria sinensisN/AYβ-phenylethyl alcoholChina[80]
Fusarium solaniGyrinops versteegiiN/AYSesquiterpen, chromones, aromatic, fatty acid, triterpenIndonesia[81]
Fusarium solaniAquilaria malaccensisN/AYSesquiterpen, chromones, aromatic, fatty acid, triterpenIndonesia[81]
Aspergillus nigerGyrinops wallaAgarwood samplesYJinkohol, agarospirol and 2(2-phenyl) chromone derivatives, b-Seline, γ-eudesmol and valerenal, γ-ElemeneSri Lanka[28]
Fusarium solaniGyrinops wallaAgarwood samplesYJinkohol, agarospirol and 2(2-phenyl) chromone derivatives, b-Seline, γ-eudesmol and valerenal, γ-ElemeneSri Lanka[28]
Lasiodiplodia aquilariaeAquilaria crassnaAgarwood samplesNN/ALaos[3]
Lasiodiplodia brasiliensisAquilaria crassnaAgarwood samplesNN/ALaos[3]
Lasiodiplodia curvataAquilaria crassnaAgarwood samplesNN/ALaos[3]
Lasiodiplodia irregularisAquilaria crassnaHealthy tissueNN/ALaos[3]
Lasiodiplodia laosensisAquilaria crassnaHealthy tissueNN/ALaos[3]
Lasiodiplodia lignicolaAquilaria crassnaAgarwood samplesNN/ALaos[3]
Lasiodiplodia macroconidicaAquilaria crassnaAgarwood samplesNN/ALaos[3]
Lasiodiplodia microcondiaAquilaria crassnaHealthy tissueNN/ALaos[3]
Lasiodiplodia pseudotheobromaeAquilaria crassnaHealthy tissue and Agarwood samplesNN/ALaos[3]
Lasiodiplodia sp.Aquilaria crassnaHealthy tissue and Agarwood samplesNN/ALaos[3]
Lasiodiplodia tenuiconidiaAquilaria crassnaAgarwood samplesNN/ALaos[3]
Lasiodiplodia tropicaAquilaria crassnaHealthy tissueNN/ALaos[3]
Fusarium solaniAquilaria sinensisN/AYN/AChina[82]
Lasiodiplodia theobromaeAquilaria sinensisN/AYN/AChina[82]
Fusarium solaniGyrinops versteegiiN/AY(1) alloaromadendrene. (2) β-eudesmol. (3) β-selinene. (4) chromone derivatives 2-(2-phenylethyl) chromen-4-one. (5) 6-methoxy-2-(2-phenylethyl) chromen-4-one. (6) 6,7-dimethoxy-2-(2-phenylethyl) chromen-4-one.Indonesia[26]
Alternaria sp.Aquilaria malaccensisJuvenile (1-year-old) woodsNN/AIndia[83]
Cladosporium sp.Aquilaria malaccensisAgarwood samplesNAntibacterial effect against Escherichia coli and Bacillus subtilisIndia[83]
Curvularia sp.Aquilaria malaccensisJuvenile (1-year-old) woodsNN/AIndia[83]
Fusarium sp.Aquilaria malaccensisAgarwood samplesNN/AIndia[83]
Penicillium sp.Aquilaria malaccensisAgarwood samplesNN/AIndia[83]
Rhizopus sp.Aquilaria malaccensisJuvenile (1-year-old) woodsNN/AIndia[83]
Sterilia sp.Aquilaria malaccensisJuvenile (1-year-old) woodsNN/AIndia[83]
Nemania aquilariaeAquilaria sinensisAgarwood samplesN(1) Bicyclo[3.1.1]hept-3-ene-2-acetaldehyde, 4,6,6-trime-thyl-, (1R,2R,5S) rel-. (2) Naphthalene,1,2,3,4,4a,5,6,7-octahydro-4a,8-dimethyl-2-(1-meth-ylethenyl)-. (3) Alloaromadendrene. (4) Valencen. (5) α-Selinene. (Antibacterial and antimicrobial)China[25]
Nemania yunnanensisAquilaria sinensisAgarwood samplesNN/AChina[25]

2. Conclusions

In this review, the potential of artificial induction of agarwood through endophytic fungi in agarwood plants is discussed. In addition, the biological activities of endophytic fungi in agarwood plants are also reviewed. The high commercial demand for agarwood, agarwood essential oil, and agarwood-based products puts the natural agarwood-producing plants under higher threat [21]. Under the sustainable utilization of natural products, the commercial cultivation of agarwood-producing plants became important. Maintenance of higher quality is important to sustain a high level of marketability of agarwood products. The artificial induction of agarwood production became a “hot topic” among natural product researchers, especially at the beginning of the 21st century (Table 1). Most of this research was focused on the biological induction of agarwood production due to the beneficial effects. As a result of the trend towards biological induction of agarwood production, many studies were carried out to understand the fungal community present in the agarwood plants and their potential for agarwood production. A majority of studies have been focused on artificial infection of endophytic fungal strains to plants. According to the literature, 171 strains have been identified from agarwood plants, of which 59 strains have been demonstrated to induce the production of agarwood, and out of 59 strains, 28 strains belong to the family Nectriaceae (47.5%). This reflects that ascomycetous fungi belonging to the Nectriaceae have the highest potential for the artificial induction of agarwood (Table 2). Studies of endophytic fungal populations in agarwood have revealed many interesting biological properties. Based on the literature, 38 strains of a total of 171 strains were investigated for their biological properties, which is 22.2% of the known assemblage of endophytic fungi associated with agarwood plants (Table 1 and Table 3).
Fungal inoculation for inducing agarwood resin production has been demonstrated to be effective, and the quality of the induced agarwood and natural agarwood are highly similar. Biological induction is faster than physical induction and safer than chemical induction. Therefore, it is necessary to further study endophytic fungi. The latest research shows that saprophytic bacteria (Bacillus) release the effective components of agarwood by degrading cellulose, which provides more evidence for future research [84]. Currently, studies on the fungal communities of agarwood mainly focus on endophytic fungi, while only a few reports have been published on saprophytic fungi. The research of Yang et al. [84] inspired researchers to carry out studies on saprophytic fungi in the future, in addition to in-depth research on endophytic fungi. Hence, for the sustainable development of the agarwood industry, further research is necessary to identify the endophytic fungal communities of agarwood plants that can be used to induce agarwood. The inoculation potential of non-pathogenic agarwood inducers is important. Proper research studies on the natural pathogens of agarwood trees, effective endophytic strains and effective saprobic strains must be carried out. Commercial agarwood production needs more scientific attention for the sustainability of the future agarwood industry and for environmental protection.

Author Contributions

Conceptualization, S.C.K. and S.T.; methodology, S.T. and T.-Y.D.; software, T.-Y.D.; validation, S.C.K. and S.T.; formal analysis, S.C.K., S.T. and T.-Y.D.; investigation, C.-J.D. and T.-Y.D.; resources, S.C.K., S.T. and T.-Y.D.; writing—original draft preparation, C.-J.D. and T.-Y.D.; writing—review and editing, A.M., A.M.E., C.-J.D., N.S., S.A.-R., S.C.K., S.L.S., S.T. and T.-Y.D.; visualization, S.C.K., S.T. and T.-Y.D.; supervision, S.C.K. and S.T.; project administration, S.C.K. and S.T.; funding acquisition, S.C.K. and S.T. All authors have read and agreed to the published version of the manuscript.


The authors extend their appreciation to the Researchers Supporting Project number (RSP-2021/120), King Saud University, Riyadh, Saudi Arabia. This research work was partially supported by Chiang Mai University.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.


We are grateful to Kevin D. Hyde for his guidance and help.

Conflicts of Interest

The authors declare no conflict of interest.


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Figure 1. Methods of artificial induction of agarwood resin. A Physical injury [38], B Chemical inducer [12], C Biological inoculation (fungal inoculation) [28].
Figure 1. Methods of artificial induction of agarwood resin. A Physical injury [38], B Chemical inducer [12], C Biological inoculation (fungal inoculation) [28].
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Figure 2. Endophytic fungi isolated from various parts of agarwood-producing trees.
Figure 2. Endophytic fungi isolated from various parts of agarwood-producing trees.
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Table 2. Endophytic fungi that have been shown to induce the formation of agarwood. “N/A” indicates no information available.
Table 2. Endophytic fungi that have been shown to induce the formation of agarwood. “N/A” indicates no information available.
Endophytic Fungi SpeciesEndophytic Fungi FamilyAgarwood-Producing TreesCountryReferences
Acremonium sp.Incertae sedisAquilaria crassnaN/A[56]
Acremonium sp.Incertae sedisAquilaria microcarpaMalaysia[50]
Aspergillus nigerAspergillaceaeGyrinops wallaSri Lanka[28]
Aspergillus sp.AspergillaceaeAquilaria sp.India[58]
BotryodyplodisN/AAquilaria sp.India[58]
Botryosphaeria dothideaBotryosphaeriaceaeAquilaria sp.India[58]
Botryosphaeria sp.BotryosphaeriaceaeAquilaria sinensisChina[32]
Chaetomium globosumChaetomiaceaeAquilaria agallochaIndia[47]
Chaetomium globosumChaetomiaceaeAquilaria agallochaN/A[49]
Cladosporium sp.CladosporiaceaeAquilaria agallochaN/A[61]
Diplodia sp.BotryosphaeriaceaeAquilaria sp.India[58]
Epicoccum granulatumDidymellaceaeAquilaria agallochaIndia[60]
Fusarium bulbigeniumNectriaceaeAquilaria sp.N/A[63]
Fusarium lateritiumNectriaceaeAquilaria sp.N/A[63]
Fusarium moniliformeNectriaceaeAquilaria sp.N/A[51]
Fusarium oxysporumNectriaceaeAquilaria agallochaIndia[47]
Fusarium oxysporumNectriaceaeAquilaria agallochaN/A[49]
Fusarium oxysporumNectriaceaeAquilaria sinensisChina[74]
Fusarium oxysporumNectriaceaeAquilaria sinensisChina[79]
Fusarium oxysporumNectriaceaeAquilaria sp.N/A[63]
Fusarium sambucinumNectriaceaeAquilaria sp.N/A[51]
Fusarium solaniNectriaceaeAquilaria malaccensisIndonesia[44]
Fusarium solaniNectriaceaeAquilaria malaccensisIndonesia[81]
Fusarium solaniNectriaceaeAquilaria sinensisChina[24]
Fusarium solaniNectriaceaeAquilaria sinensisChina[82]
Fusarium solaniNectriaceaeAquilaria sp.N/A[51]
Fusarium solaniNectriaceaeGyrinops versteegiiIndonesia[81]
Fusarium solaniNectriaceaeGyrinops versteegiiIndonesia[26]
Fusarium solaniNectriaceaeGyrinops wallaSri Lanka[28]
Fusarium sp.NectriaceaeAquilaria beccarianaN/A[53]
Fusarium sp.NectriaceaeAquilaria crassnaN/A[56]
Fusarium sp.NectriaceaeAquilaria malaccensisIndia[78]
Fusarium sp.NectriaceaeAquilaria malaccensisN/A[55]
Fusarium sp.NectriaceaeAquilaria microcarpaN/A[52]
Fusarium sp.NectriaceaeAquilaria sinensisChina[32]
Fusarium sp.NectriaceaeAquilaria sinensisChina[77]
Fusarium sp.NectriaceaeAquilaria sp.Indonesia[48]
Fusarium sp.NectriaceaeAquilaria sp.Sumatra island[48]
Fusarium sp.NectriaceaeGyrinops versteegiiIndonesia[48]
Fusarium tricinctumNectriaceaeAquilaria sp.N/A[51]
Lasiodiplodia sp.BotryosphaeriaceaeAquilaria sinensisChina[45]
Lasiodiplodia theobromaeBotryosphaeriaceaeAquilaria sinensisChina[29]
Lasiodiplodia theobromaeBotryosphaeriaceaeAquilaria sinensisChina[74]
Lasiodiplodia theobromaeBotryosphaeriaceaeAquilaria sinensisChina[24]
Lasiodiplodia theobromaeBotryosphaeriaceaeAquilaria sinensisChina[77]
Lasiodiplodia theobromaeBotryosphaeriaceaeAquilaria sinensisChina[79]
Lasiodiplodia theobromaeBotryosphaeriaceaeAquilaria sinensisChina[82]
Melanotus flavolivensStrophariaceaeAquilaria sinensisChina[30]
Melanotus flavolivensStrophariaceaeAquilaria sinensisChina[65]
Nigrospora oryzaeIncertae sedisAquilaria sinensisChina[80]
Paraconiothyrium variabileDidymosphaeriaceaeAquilaria sinensisChina[71]
Rigidoporus vinctusMeripilaceaeAquilaria sinensisChina[46]
Torula sp.TorulaceaeAquilaria agallochaN/A[61]
Unidentified five fungi belonging to the Deuteromycetes and Ascomycetes groupsN/AAquilaria malaccensisMalaysia[54]
Xylaria sp.XylariaceaeAquilaria sinensisChina[45]
Table 3. Bioactivity of endophytic fungi isolated from agarwood-producing trees. “N/A” indicates no information available.
Table 3. Bioactivity of endophytic fungi isolated from agarwood-producing trees. “N/A” indicates no information available.
Endophytic Fungi SpeciesEndophytic Fungi FamilyIsolation SourceBioactivityReferences
Botryosphaeria rhodinaBotryosphaeriaceaeAquilaria sinensisAntimicrobial activity[64]
Cephalosporium sp.Incertae sedisAquilaria sinensisAntimicrobial activity[64]
Cladophialophora sp.HerpotrichiellaceaeAquilaria sinensisAntimicrobial activity[64]
Cladosporium edgeworthraeCladosporiaceaeAquilaria sinensisAntimicrobial activity[64]
Cladosporium sp.CladosporiaceaeAquilaria malaccensisAntibacterial effect against Escherichia coli and Bacillus subtilis[83]
Cladosporium tenuissimumCladosporiaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Colletotrichum sp.GlomerellaceaeAquilaria sinensisAntimicrobial activity[64]
Coniothyrium nitidaeConiothyriaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Diaporthe sp.DiaporthaceaeAquilaria subintegraExcellent antioxidant capacity[31]
Epicoccum nigrumDidymellaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Epicoccum sp.DidymellaceaeAquilaria sinensisAntimicrobial activity[64]
Fusarium equisetiNectriaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Fusarium oxysporumNectriaceaeAquilaria sinensisAntimicrobial activity[64]
Fusarium oxysporumNectriaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Fusarium solaniNectriaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Fusarium sp.NectriaceaeAquilaria sinensisAntimicrobial activity[64]
Fusarium verticillioidesNectriaceaeAquilaria crassnaAntimicrobial activity[76]
Geotrichum candiumDipodascaceaeAquilaria crassnaAntimicrobial activity[76]
Geotrichum sp.DipodascaceaeAquilaria sinensisAntimicrobial activity[64]
Glomerularia sp.PlatygloeaceaeAquilaria sinensisAntimicrobial activity[64]
Gonytrichum sp.ChaetosphaeriaceaeAquilaria sinensisAntimicrobial activity[64]
Guignardia manqiferaePhyllostictaceaeAquilaria sinensisAntimicrobial activity[64]
Hypocrea lixiiHypocreaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Lasiodiplodia theobromaeBotryosphaeriaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Leptosphaerulina chartarumDidymellaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Monilia sp.SclerotiniaceaeAquilaria sinensisAntimicrobial activity[64]
Mortierella sp.MortierellaceaeAquilaria sinensisAntimicrobial activity[64]
Mycelia sterilia sp.N/AAquilaria sinensisAntimicrobial activity[64]
Nemania aquilariaeXylariaceaeAquilaria sinensisAntibacterial and antimicrobial[25]
Ovulariopsis sp.ErysiphaceaeAquilaria sinensisAntimicrobial activity[64]
Paraconiothyrium variabileDidymosphaeriaceaeAquilaria sinensiAntimicrobial and antitumor activity[68]
Penicillium sp.AspergillaceaeAquilaria sinensisAntimicrobial activity[64]
Phaeoacremonium rubrigenumTogniniaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Phoma herbarumDidymellaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Pleospora sp.PleosporaceaeAquilaria sinensisAntimicrobial activity[64]
Rhinocladiella sp.HerpotrichiellaceaeAquilaria sinensisAntimicrobial activity[64]
Rhizomucor variabilisLichtheimiaceaeAquilaria sinensisAntimicrobial and antitumor activity[68]
Xylaria maliXylariaceaeAquilaria sinensisAntimicrobial and antitumor activity[32]
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Du, T.-Y.; Dao, C.-J.; Mapook, A.; Stephenson, S.L.; Elgorban, A.M.; Al-Rejaie, S.; Suwannarach, N.; Karunarathna, S.C.; Tibpromma, S. Diversity and Biosynthetic Activities of Agarwood Associated Fungi. Diversity 2022, 14, 211.

AMA Style

Du T-Y, Dao C-J, Mapook A, Stephenson SL, Elgorban AM, Al-Rejaie S, Suwannarach N, Karunarathna SC, Tibpromma S. Diversity and Biosynthetic Activities of Agarwood Associated Fungi. Diversity. 2022; 14(3):211.

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Du, Tian-Ye, Cheng-Jiao Dao, Ausana Mapook, Steven L. Stephenson, Abdallah M. Elgorban, Salim Al-Rejaie, Nakarin Suwannarach, Samantha C. Karunarathna, and Saowaluck Tibpromma. 2022. "Diversity and Biosynthetic Activities of Agarwood Associated Fungi" Diversity 14, no. 3: 211.

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