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11 March 2022

Diversity and Biosynthetic Activities of Agarwood Associated Fungi

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1
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing 655011, China
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Centre of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
3
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
4
College of Resources and Environment, Yunnan Agricultural University, 452 Fengyuan Road, Kunming 650201, China
Diversity2022, 14(3), 211;https://doi.org/10.3390/d14030211
This article belongs to the Topic Fungal Diversity
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Abstract

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 (https://tmhagarwood.com/agarwood-prices-updated-in-2021, 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).
Figure 1. Methods of artificial induction of agarwood resin. A Physical injury [38], B Chemical inducer [12], C Biological inoculation (fungal inoculation) [28].

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).
Figure 2. Endophytic fungi isolated from various parts of agarwood-producing trees.
Table 2. Endophytic fungi that have been shown to induce the formation of agarwood. “N/A” indicates no information available.
Table 3. Bioactivity of endophytic fungi isolated from agarwood-producing trees. “N/A” indicates no information available.
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).

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.

Funding

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.

Data Availability Statement

Not applicable.

Acknowledgments

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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