Abstract
The inhibitory ability of Fokienia hodginsii heartwood (FHH) extracts on Trametes versicolor (TV) and Gloeophyllum trabeum (GT) as well as the toxic effect of its heartwood extracts on GT were studied. The growth inhibition ability of the samples was analyzed using the growth rate method. The results showed that in the experiment of inhibiting TV, extracts using hot water had little effect, acetone extracts had the best inhibiting effect, and the lowest value of acetone EC50 was 0.409 g/L. The parameter EC50 is the concentration of the corresponding agent that inhibits the growth of 50% fungi. In the antifungal experiment of GT, methanol extract had the best inhibition effect, and the lowest EC50 value was 0.283 g/L. The antifungal effect of five solvent extracts of FHH was good when the concentration was 10% (w/w), and at this time, the mass loss rate of the test pieces was below 11%, all of them were Class I, indicating a strong antifungal level. After observing the samples of GT with SEM, it was found that the structure of methanol extract treatment was more complete and the antiseptic effect was better than that of the hot water extract treatment.
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Antifungal Ability and Decay Resistance of Fokienia hodginsii Heartwood Extract and its Inhibitory Effect on Gloeophyllum trabeum
Jian-Fei Wu,a Xue-Feng Zhuang,a Hong-mei Yuan,a Quan Li,a,b Wei Wang,a Ji-Qing Li,a,* and Jin-Guo Lin a
The inhibitory ability of Fokienia hodginsii heartwood (FHH) extracts on Trametes versicolor (TV) and Gloeophyllum trabeum (GT) as well as the toxic effect of its heartwood extracts on GT were studied. The growth inhibition ability of the samples was analyzed using the growth rate method. The results showed that in the experiment of inhibiting TV, extracts using hot water had little effect, acetone extracts had the best inhibiting effect, and the lowest value of acetone EC50 was 0.409 g/L. The parameter EC50 is the concentration of the corresponding agent that inhibits the growth of 50% fungi. In the antifungal experiment of GT, methanol extract had the best inhibition effect, and the lowest EC50 value was 0.283 g/L. The antifungal effect of five solvent extracts of FHH was good when the concentration was 10% (w/w), and at this time, the mass loss rate of the test pieces was below 11%, all of them were Class I, indicating a strong antifungal level. After observing the samples of GT with SEM, it was found that the structure of methanol extract treatment was more complete and the antiseptic effect was better than that of the hot water extract treatment.
Keywords: Fokienia hodginsii; Extract; Gloeophyllum trabeum; Inhibition; SEM observation; antifungal; Trametes versicolor
Contact information: a: College of Material Engineering, Fujian Agriculture and Forestry University, Fuzhou 35002, Fujian, China; b: Kaili University, Kaili 556011, Guizhou, China;
* Corresponding authors: nfuljq@163.com; fjlinjg@126.com
INTRODUCTION
Fungi, such as white-rot fungi and brown-rot fungi, can seriously decompose and destroy wood. The Trametes versicolor (TV) studied in this work is a type of white-rot fungus and Gloeophyllum trabeum (GT) is a type of brown-rot fungus. Under suitable conditions, they use lignin, cellulose, and hemicellulose as nutrients. They spread and infect in the form of spores, causing wood rot. Antifungal active ingredients are present in various plants in nature, such as trees, and these antifungal active ingredients are plant extracts (Alvarez-Castellanos et al. 2001; Barron et al. 2003; Bajpai et al. 2008; Ahnet et al. 2010; Bhardwaj et al. 2012). Studies have shown that extracts from more than 40 plants have varying degrees of antifungal effects, including extracts from spruce, larch, peach, juniper, olive, litchi, poplar, African hardwood, toothbrush tree, citrus, rubber wood, etc. (Özkan et al. 2015; Peng et al. 2015; Salem et al. 2016; Yang et al. 2016; EL-Hefny et al. 2017; Onuorah et al. 2002; Abhary and Al-Hazmi 2016; Okla et al. 2019; Vainio-Kaila et al. 2015; Uyup et al. 2019). Some of these antifungal substances can be secreted directly on the surface of plants. Nakayama (2005) in the United States reported that some plants, such as silver geranium, sugar cane, etc., secreted resin components that have an antifungal function (Oumzil et al. 2002; Tascioglu et al. 2013). However, in fact, most of the antifungal components exist in the plant body and need to be extracted with a solvent such as ethanol. Eller et al. (2010) treated wood samples with extracts from North American juniper using liquid carbon dioxide and ethanol. The extracts were tested for fungal decay and insect resistance. Nanasombat et al. (2018) determined the antifungal activity of methanol extracts from 25 Thailand medicinal plants against 10 strains of fungi. The results showed that ethanol and other organic solvents were suitable for the extraction of antifungal substances in plants. The concentration of FHH extract is relatively low, and some people used to worry that this would affect its antifungal effect. In recent years, scientists have evaluated the antifungal and antimicrobial activities of two types of pyroic acid (PA), and studies have shown that both types of PA inhibit all microorganisms even at a minimum concentration of 20% (De Souza Araujo et al. 2017). This suggests that concentration is not the most important determinant of antifungal substances. Because the heartwood has better antifungal properties than sapwood, FH’s heartwood was selected in the present work as the material. (Cheng et al. 2003; Harju et al. 2003; Gierlinger et al. 2004; Chua et al. 2008).
There are many types of cypress trees, and the effects of cypress extracts have been studied for a long time. For example, Noruzi et al. (2012) used cypress extract for the synthesis of gold nanoparticles. Shahali et al. (2009) studied the response of immunoglobulin E to cypress pollen extract. Takaiwa and Yang (2014) developed a vaccine against cypress pollen. Many cypress extracts also have antifungal effects, and Fokienia hodginsii (FH) is one of them. FH is a kind of cypress tree with straight trunks, solid material, and strong decay resistance. It is often used in architecture and furniture. It is distributed in southern China provinces, such as Fujian, Sichuan, Yunnan, and Guangdong, and belongs to the national ‘second-class’ of endangered plants. At the same time, the aromatic oil of FH has antifungal and anti-tumor effects, and it can also be used as a spice for making soap. The FH has a strong resistance to fungal decay. At present, people know little about the tree. Therefore, the inhibitory effect of Fokienia hodginsii heartwood (FHH) extract on TV and the GT and the toxic effect of the heartwood extract on the GT were studied. It is of great importance for understanding the antifungal and antiseptic mechanism of FHH. This research also has important practical application value for the rational utilization of the wood processing residues, such as scrap, sawdust, and saw powder by FH, in its production and processing.
EXPERIMENTAL
Materials
Test species
The FHH scrap and sawdust were taken from the forest products market of Shunchang County, Nanping City, Fujian Province, China. A small amount of FHH were dried and sawn into 20 mm × 20 mm × 10 mm specimens in the direction of the grain for the determination of natural decay resistance. Most of the cedar heartwood scraps and sawdust were air-dried, crushed, sieved with a pulverizer, and screened to 40- to 60-mesh wood powder as the raw material for the test. Finally, the obtained FHH powder was placed in the freezer and sealed for use. Masson pine, taken from Shunchang County, Fujian Province, had a tree age of 20 to 25 years. Because masson pine is easily degraded by brown-rot fungus, it is meaningful to study its fungal decay resistance level. The feeding wood for the natural wood test and the preservative toxicity test was 20 mm × 20 mm × 10 mm, and was fed the direction of the grain.
Test strains
The white-rot fungi Trametes versicolor was supplied by the China Forestry Microbial Culture Collection Management Center (Beijing, China). The brown-rot fungus Gloeophyllum trabeum was supplied by the College of Life Sciences of Fujian Agriculture and Forestry University (Fuzhou, China).
Solvents and other materials
Hot water was made by adding tap water to the distillation flask, then adding some broken porcelain pieces, and then plugging it with a rubber plug inserted with a thermometer. The distillation flask was heated. When the water temperature reached approximately 100 °C, the water was boiled, and the water vapor was collected through the condensation tube after condensation in the bottle. The methanol, chloroform, acetone, petroleum ether, ethyl acetate, all of analytical pure and obtained from Tianjin Fuyu Fine Chemical Co., Ltd. (Tianjin, China); the agar, maltose, and potatoes, etc. were purchased from the local market.
Preparation of maltose agar medium
After peeling the potatoes, they were chopped and soaked in hot water. Subsequently, 200 g of potatoes, 15 g of agar, 20 g of maltose were weighed, and 1000 mL of hot water was weighed, dissolved by heating, filtered, and then diluted to a volume of 1000 mL. Then, 150 mL of medium was placed in 6 conical flasks. The flasks were placed in the steam sterilizer, where they were subjected to high pressure moist heat sterilization for 30 min at 121 °C.
Methods
Instruments and equipment
The scanning electron microscope (SEM) was mainly used to observe the microstructure of samples (FEI-Quanta-200; FEI Company, Hillsborough, OR, USA). The magnification level was 100 times and 500 times to observe the sample. Samples were dried with a blast dryer at 45 °C (DHG-9246A; Shanghai Jinghong Experimental Equipment Co., Ltd., Shanghai, China). Strains were cultured in a humidified incubator with a temperature of 28 °C and a humidity of 80% (HW-150; Shanghai Jinghong Experimental Equipment Co., Ltd., Shanghai, China).
The virulence regression equation was calculated using Microsoft Office 2010 (Microsoft Corporation, Redmond, WA, USA), the experimental further explains for the specific calculation process. The correlation coefficient R was obtained by the CORREL function, and then R2 was obtained.
Preparation of extracts
The mixture was subjected to hot reflux extraction using a condenser; approximately 100 g of the 40- to 60-mesh-sized FHH wood powder was placed in a round bottom flask and extracted with one of six different kinds of organic solvents. The extraction was completed in two portions, and the extraction was performed for the first time according to the ratio of the raw material to the solvent of 1:7 (g/mL) for 5 h, followed by removal of the filtration. The second extraction was performed for 3 h according to the ratio of the raw material to the solvent of 1:5 (g/mL), followed by filtration. Next, the two filtrates were mixed and evaporated under reduced pressure with a rotary evaporator to obtain a paste. Subsequently, the paste was dissolved in 6 different solutions to prepare the samples and then placed in a refrigerator at 4 °C for future use.
Determination of the antifungal activity of extracts
The growth rate of the toxic medium culture method (Huang 1993) was used to determine the inhibition effects of the six chemical solvents of the FHH extract relative to the growth of TV and GT. First, the two wood-decay fungi were cultured on a potato dextrose agar (PDA) plate for 7 days, and the sterilized medium was heated, melted, and cooled to approximately 50 °C. A certain amount of medium was placed in the culture dish, and then pipetted to separately measure the test sample into a sterile Petri dish, where it was shaken. The concentrations of the six medicated media for inhibiting TV are shown in Table 1. The concentrations of the six solvent-containing media for inhibiting brown-rot fungi are shown in Table 2, and blank control group was also set. Then, the inoculation test was performed. A hole cutter was used with a diameter of 7.0 mm to make the mushroom cake at the edge of the colony, and the inoculating ring was used to move fungi to the center of the above six culture dishes (one of them was a blank control). To avoid the inhibition of the two fungi by chemical solvents, 1 mL of each of the different extraction reagents was added to each of the six culture dishes. During the experiment, it was found that a trace amount of methanol solvent highly inhibited the two wood-decaying fungi, so the methanol solvent in the drug-containing medium was volatilized before it was transferred to the mycelium block. The test was repeated three times, and then the culture dish was placed in a constant temperature and humidity incubator at a temperature of 28 °C and humidity of 80%. If the hyphae in the culture dish of the control group grew to approximately two-thirds of the diameter of the culture dish, the growth diameter of the colony was measured by the cross method, and the average value was calculated. The inhibition rate (IR) was calculated according to Eq. 1:
Table 1. Inhibiting the Concentration of Drug-containing Medium in Each Solvent of TV
Table 2. Inhibiting the Concentration of Each Solvent-containing Medium in the GT
The EC50 value of virulence is the concentration of a poison that causes some harm to half of the test subjects over a certain period of time. In this paper, EC50 refers to the concentration of the corresponding agent that inhibits the growth of 50% fungi. If the measured value is smaller than EC50, then the antifungal ability of the agent is stronger. The calculation of virulence EC50 value is as follows. Calculate the probability value corresponding to each bacteriostatic rate from the conversion relationship between the bacteriostatic rate and the probability value. Then, use the logarithmic value to indicate the concentration. The logarithmic value (x) at each concentration of each chemical solvent extract is subtracted from the probability value (y). Then, the virulence regression equation is obtained (i.e., y = a + bx), and the toxic EC50 value that inhibits mycelial growth is calculated (Chattapadhyay et al. 2006).
Natural durability test
According to Chinese Standard GB/T 13942.1 (2009), the decay resistance test of FHH was performed. The mass loss rate (T) was calculated after decay of each test piece and expressed as a percentage. The natural decay resistance loss rate percentage T is given by Eq. 2,
(2)
where W1 is the completely dry mass before the test piece (g), and W2 is the completely dry mass after the test piece (g).
Preparation of preservatives
The six solvent extracts (methanol extract, ethyl acetate extract, acetone extract, chloroform extract, petroleum ether extract, and distilled water extract) were dissolved in corresponding solvents to prepare test solutions at the concentrations of 10%, 8%, 6%, 4%, and 2% (w/w). Amine copper quaternary (ACQ) was mixed with distilled water to prepare the drug solutions with a concentration of 2%, 1%, 0.5%, 0.25%, and 0.125%.
Preservative toxicity test
The toxicity determination test was performed according to Chinese Standard LY/T 1283 (2011). The drug loading (R) of the preservative for each sample (kg/m3) was calculated according to Eq. 3,
(3)
where m1 is the constant mass of the test piece before the preservative is absorbed (g), m2 is the quantity of the specimen immediately weighed after the preservative is absorbed (g), C is the preservative solution concentration (% mass fraction), and V is the sample volume (cm3).
The percentage of mass loss (L) was calculated after the decay of each test piece using Eq. 4,
(4)
where L is the test piece mass loss rate (%), m3 is the constant mass of the test piece before decay (g), and m4 is the constant mass of the test piece after decay (g).
Experimental conditions of SEM
10% methanol extract solution was sprayed on the surface of FHH. The other group was exposed to 10% hot water extract, which was sprayed on the surface of FHH. There was also a blank control group. The sample was placed in a blast oven, the temperature was set to 45 °C, and dried until a constant mass was obtained. Then, the sample was cut into thin slices, the sample was pasted on the sample stage, and the sample was gold sputtered (Spray Konica Minolta MCM-200; Beijing Hanmeng Zixing Instrument Co., Ltd., Beijing, China). Finally, the samples were imaged with different SEM magnifications.
RESULTS AND DISCUSSION
FH Extract Yield and Paste Color
The yields of the six solvent extracts and the color of the paste materials are shown in Table 3. In addition to hot water, the yield of the extract was positively correlated with the polarity of the solvent in the six solvents, namely that methanol was higher than acetone > ethyl acetate > chloroform; the extract obtained from the non-polar solvent, petroleum ether, was the lowest.
Table 3. FH Extract Yield (% of Raw Materials) and Paste Color
Determination of the Activity of Two Kinds of Fungi by FHH Extract
From the inhibition rate of the extracts shown in Fig. 1 on white-rot fungi, it can be concluded that in addition to hot water, the five solvent extracts of FHH had different degrees of inhibiting TV. In general, the inhibitory effects of the five solvent extracts increased with the concentration of the drug solution; inhibition was positively correlated with the concentration, because a higher concentration resulted in more antifungal components present in the drug-containing medium. At a concentration of 0.5 g/L, the inhibition percentages of acetone, ethyl acetate, methanol, petroleum ether, and chloroform extract on the TV were 48.5%, 47.7%, 42.1%, 37.0%, and 35.9%, respectively. Among them, the FHH extract from three solvents, such as acetone, ethyl acetate, and methanol, had an inhibition rate of 50% for TV, and the inhibition rate at the same concentration was appreciably higher than the other two chemical extracts.
Fig. 1. Antifungal activity of different solvent extracts against TV
Fig. 2. Antifungal activity of different solvent extracts against G. trabeum
Based on the results shown in Fig. 2, the six kinds of reagent extracts of the FH heartwood had inhibitory effects on the viscous fungi, except for the hot water extracts. The inhibition percentages of methanol, petroleum ether, acetone, ethyl acetate, and chloroform extracts against brown-rot fungi at a concentration of 0.5 g/L were 64.0%, 54.8%, 48.0%, 45.1%, and 34.8%, respectively. Overall, the inhibitory effects of the reagent extracts with methanol, petroleum ether, acetone, ethyl acetate, and chloroform increased with increasing concentration.
Determination of the Effects of the Extract of FHH on the TV and the GT
The inhibitory effects of different solvent extracts of FHH to TV (Table 4) showed that the concentration of five extracts of FHH was positively correlated with the antifungal effect. The coefficient of determination, R2 (Microsoft Office 2010, Microsoft, Office 2010, Redmond, WA, USA), of the virulence regression equation was greater than 0.9. With the increase of extract concentration, the inhibitory effect of the extract on the TV was gradually enhanced.
The EC50 values of the five solvent extracts of FH against TV were in the range of 0.409 to 0.690 g/L. According to the EC50 value, the order of inhibition (from highest to lowest) of the five solvent extracts of cedar heartwood on C. versicolor was acetone extract, methanol extract, ethyl acetate extract, chloroform extract, and petroleum ether extract. The hot water extract had no substantial bacteriostatic action. In the wood antifungal application, for the TV EC50 value, the optimum solvent for the extraction of FHH was acetone. However, compared to the traditional wood preservative, ACQ, the EC50 value of acetone extract was much greater than that of ACQ (Li and Yan 2005).
Table 4. Inhibitory Effects of Various Solvent Extracts of FHH toward TV
It can be seen from Table 5 that the coefficients of determination (R2) of the virulence regression equations of the five solvents (excluding hot water) were more than 0.9; the bacteriostatic effect was positively correlated with the extract concentration. The EC50 values of the five extracts against GT were 0.283 to 0.856 g/L. According to the EC50 value, the order of inhibition (from highest to lowest) of brown-rot fungi by the organic solvent extracts of FHH was methanol extract, petroleum ether extract, acetone extract, ethyl acetate extract, and chloroform extract. According to the measurement results of the GT, it was found that the optimum solvent was methanol. However, the EC50 value of methanol extract was greater than ACQ (Li et al. 2014) and this extract’s antifungal ability was relatively weak when compared to ACQ.
Table 5. Virulence of Various Solvent Extracts of FH
FH Natural Decay Resistance Test Results
Sample mass loss rate
It can be seen from Table 6 that the quantity loss rate of the FHH sample after rotting from TV exposure was 6.9% (which was less than 11%) and the mass loss rate of the FHH material was 8.2% (which was less than 11%) after GT exposure. According to Chinse Standard GB/T 13942.1 (2009), FHH can be graded as a class I of best decay resistance.
Table 6. Mass Loss Rate of FHH Samples After Decay by TV and GT
SEM observation before and after the fungal decay of the sample
Fig. 3. SEM images of FHH: A: 100× magnification; B: 500× magnification
Fig. 4. SEM images of FHH after fungal decay: C: GT, 500× magnification; D: TV, 500× magnification
The samples before and after brown rot of FHH were observed. Figure 3 shows that the surfaces of the FH sample were flat, and its various structures were observed to be complete and compact at 100× and 500× magnification, respectively. Figure 4 (C) shows the FH specimens were eroded by the TV. Mycelia were visible on the surface, especially at the rupture. It can be observed that the boundary between the rupture and the fibers was destroyed. The sample was attacked to some extent. Figure 4 (D) shows the FH specimens were eroded by TV. The surface was also covered with some hyphae, but the internal hyphae were few, the structure was relatively intact, and the original shape was well maintained. The results showed that the destructive ability of TV to FHH was weaker than that of GT. In general, both of these fungi were less damaging to FHH. These observation results were consistent with the previous mass loss rate test results, which indicated that FH extract imparts good rot resistance.
Preservative Toxicity Test Results
Sample preservative retention
According to the method of a preservative-loaded drug in Chinese Standard LY/T 1283 (2011), the drug loading of FH extract and ACQ in the sample was calculated. The results are shown in Figs. 5 and 7. It can be seen from the figures that the drug loading of the test piece increased with the increasing concentration of the water-based preservative and the organic solvent preservative; these observations indicated that Masson pine wood has good permeability.
Fig. 5. Drug loading of Pinus massoniana wood-impregnated FH extract
Fig. 6. Mass loss rate after the treatment of the test piece of FH extract
Fig. 7. ACQ-treated specimens exposed to dense viscous fungi
Virulence effects of preservatives
It can be seen from Figs. 6 and 7 that with increased concentration of the liquid preservative of various drugs, the mass loss rate of the test piece after the FHH extract and the ACQ-treated Masson pine test piece was reduced. Results indicated that the six chemical preservatives were enhanced with increased concentration at inhibiting GT. It is shown in Table 7 that there were some differences in the preservative ability of different concentrations of FHH extract and ACQ treatments. The antifungal effect of the FH extracts of methanol, ethyl acetate, acetone, chloroform, and petroleum ether at a 10% (w/w) concentration was good, and the mass-loss rate was below 11%, which is a level I for best resistance. The mass-loss rate of the hot water extract at a concentration of 2% (w/w) was greater than 31%, which is a non-resistance (level IV of not good); the mass loss rate of the sample at a concentration of 10% was greater than 21%, which is a grade III of slightly antifungal. However, the mass-loss rate of the samples treated with the five concentrations of ACQ did not change much, and all had a rating of best resistance (level I). In terms of inhibiting the GT, the FHH extracts of the other five solvents (except for hot water) had antiseptic effects, and the antiseptic effect was closely related to the concentration. However, there was still a certain gap when compared with the resistance of ACQ.
SEM observation of the of the treated material of FHH extract
The SEM images of the brown-rot samples of 10% (w/w) concentration of cedar heartwood hot water extract-treated material and 10% (w/w) concentration of cedar heartwood methanol extract-treated material were observed. It can be seen from Fig. 8 that the sample treated by the hot water extract contained more rot, and a large amount of hyphae of the bacterium was densely formed inside the sample. The boundary between the cells was broken, and a large cavity was also formed. This indicated that the hyphae of GT critically invaded the inside of the sample of Pinus massoniana through the tissues, such as through ducts and pits.
Table 7. Antifungal Performance of FHH Extracts Preservative and ACQ Preservative Treated Material
Figure 9 shows a sample of the methanol extract-treated material after brown-rot exposure. When compared with Fig. 8, there were not as many hyphae in Fig. 9; the cell boundary damage was not obvious, and the tracheid and other structures were more complete with less damage caused by GT (i.e., better antiseptic effect). This observation was consistent with the test results of the mass-loss rate in the antifungal experiments.
Fig. 8. SEM images of the FHH hot water extract treated material after brown-rot exposure (E: 100×magnification; F: 500× magnification)
Fig. 9. SEM images of the chlorinated extract of FH after brown-rot exposure (G: 100× magnification; H: 500× magnification)
CONCLUSIONS
- Hot water extract of Fokienia hodginsii heartwood (FHH) had no inhibitory effect on Trametes versicolor. The inhibitory effects of the other five solvent extracts on T. versicolor were positively correlated as concentrations increased. The acetone extract had the highest effect. The order observed (from highest to lowest effect) was acetone extract, methanol extract, ethyl acetate extract, chloroform extract, and petroleum ether extract.
- The extract from hot water from FHH had no effect on Gloeophyllum trabeum. The inhibitory effects of the other five solvent extracts on G. trabeum were positively correlated as concentrations increased. The methanol extract had the highest resistance effect. The order observed (from highest to lowest effect) was methanol extract, petroleum ether extract, acetone extract, ethyl acetate extract, and chloroform extract.
- The natural resistance grade of FHH belongs to grade I (best resistance).
- The test results of 6 kinds of liquid preservatives on Gloeophyllum trabeum showed that the preservatives increased with increasing concentration in inhibiting Gloeophyllum trabeum. The antifungal effect of the five kinds of FHH extract at 10% (w/w) concentration was good. At this time, the mass-loss rate of the specimens was below 11%, which implies that all the specimens qualified as grade I (best resistance). The order observed (from highest to lowest) for resistance at this time was methanol extract, petroleum ether extract, acetone extract, ethyl acetate extract, and chloroform extract.
- SEM was used to inspect the samples of the Gloeophyllum trabeum treated with the methanol extract, and the findings were compared the samples of the Gloeophyllum trabeum treated with the hot water extract. It was found that the structure treated with methanol extract was more complete and the antifungal effect was relatively better. This observation was consistent with the experimental results of the mass-loss rate of the antifungal tests.
- This research demonstrated the antifungal and antifungal mechanism of FHH and provided a scientific basis for the rational use of residue extracted from FH in the production process.
ACKNOWLEDGEMENTS
The authors thank the Fujian Agriculture and Forestry University Science and Technology Innovation fund (KFA17218A, CXZX2018011, CXZX2017479). The authors also thank the Fujian Provincial Forestry Department, project K8517201A. The author also thanks the national natural science foundation of China for its support (no.31760191).
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Article submitted: November 11, 2019; Peer review completed: February 13, 2020; Revised version received: February 17, 2020; Accepted: February 18, 2020; Published: March 3, 2020.
DOI: 10.15376/biores.15.2.2784-2799