Next Article in Journal
Spatial Pattern and Competitive Relationships of Moso Bamboo in a Native Subtropical Rainforest Community
Previous Article in Journal
Variation in Climate Signals in Teak Tree-Ring Chronologies in Two Different Growth Areas
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 9
Issue 12
10.3390/f9120773
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Allelopathy of Wild Mushrooms—An Important Factor for Assessing Forest Ecosystems in Japan

by
Asma Osivand
1,
Hiroshi Araya
2,*,
Kwame S. Appiah
1,
Hossein Mardani
3,
Takayuki Ishizaki
4 and
Yoshiharu Fujii
3
1
Department United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo 183-8504, Japan
2
Department of Agrochemistry, School of Agriculture, Meiji University, Kanagawa 214-8571, Japan
3
Department International Environmental and Agricultural Science, Tokyo University of Agriculture and Technology, Tokyo 183-8504, Japan
4
Department of Agri-Production Sciences, College of Agriculture, Tamagawa University, Tokyo 194-8610, Japan
*
Author to whom correspondence should be addressed.
Forests 2018, 9(12), 773; https://doi.org/10.3390/f9120773
Submission received: 7 November 2018 / Revised: 6 December 2018 / Accepted: 11 December 2018 / Published: 14 December 2018
(This article belongs to the Section Forest Ecophysiology and Biology)
Browse Figures
Versions Notes

Abstract

:
Research Highlights: Some organisms such as plants and fungi release certain secondary metabolites, generally called allelochemicals, which can influence the organisms around them. Some of the secondary metabolites released by mushrooms may have certain effects on the growth and development of neighboring plants. Background Objectives: The purpose of the present study was to investigate the allelopathic potential of mushrooms in a forest ecosystem. To this end, 289 Japanese mushroom species were collected from the wild and tested using a modified sandwich method, which is a quick and effective bioassay technique. Materials and Methods: The collected specimens were prepared for bioassay as dried samples, and 10 mg/well (10 cm2) was added to a 6-well multidish according to the mycelia biomass, which was estimated at 700−900 kg ha−1 year−1 (7–9 mg 10 cm−2) in coniferous forests. Results: Of the screened mushroom species, 74% inhibited more than 50% of the radicle elongation in lettuce (Lactuca sativa var. Great Lakes 366) seedlings, while the average of all species was 41.1%. This result suggests that wild mushrooms have a significant regulatory effect on lettuce growth. According to our standard deviation variance analysis, 54 out of 289 species showed significant allelopathic activity. Among these species, Xeromphalina tenuipes, Cortinarius violaceus, and Clavaria miyabeana exhibited the strongest growth inhibitory activity, with radicle elongation of 5.1%, 4.3%, and 7.6% of the control, respectively. In contrast, Ischnoderma resinosum stimulated the length of radicle and hypocotyl growth by 30.6% and 42.0%, respectively. These results suggest that these species may play important roles in ecosystems. In addition, the wide range of allelopathic activities observed in mushrooms indicates that various amounts of diverse secondary metabolites from these species are involved in mushroom allelopathy. Conclusions: Our study reveals the importance of evaluating mushroom allelopathy to understand the wider ecological structures within complex ecosystems.

1. Introduction

A forest ecosystem is a complex of living organisms. All of them interact with the environment in which they live and among themselves via various bioactive chemicals [1]. Allelopathy through the release of allelochemicals is one of the ecological interactions which effects the growth and development of forest ecosystems. Allelochemicals are directly and indirectly involved in seedling growth disturbances, including the delay and reduction of germination and restriction of root development. In mature trees, mycorrhizal functions and growth stagnation may result in death and the disappearance of species in severe cases. Blanco [2] stated that plant allelopathy is an important ecological factor in forest ecosystems. Allelopathic plants may promote succession in non-native environments by possessing unique bioactive compounds [3]. Accordingly, allelopathy may be much more important as a mechanism in recipient natural plant communities because they appear to evolve tolerance to chemicals [4]. However, neither Blanco nor others have considered the allelopathy of mushrooms, including mycorrhizal fungi, as important factors. This is in spite of the substantial evidence on the interference of allelopathic mushrooms in natural ecosystems through unique allelochemicals [5,6].
Higher fungi—Ascomycetes and Basidiomycetes—interfere in many ecosystems with nearby plants, either directly or indirectly [7,8,9,10]. Basidiomycete mushroom aqueous extracts can directly inhibit/stimulate the growth and germination rates of Pinus banksiana as well as lichens, herbaceous plants, and trees [11]. Furthermore, mycorrhizal mushrooms have a symbiotic relationship with certain trees to exchange bioactive chemicals. These chemicals, when released into the environment, may show certain allelopathic effects on neighboring non-symbiotic plants [12]. Additionally, saprotrophic mushrooms produce many phenolic allelochemicals by decomposing lignin in wood litters [13]. Thus, fungal material should also be considered to gain a clearer understanding of ecosystems. Plant litter biomass accounts for approximately 1500–2500 kg ha−1 year−1 in coniferous forests [14], while the amount of ectomycorrhizal mycelia biomass has been estimated at 700–900 kg ha−1 year−1 [15]. This represents a significant source of allelochemicals which are released into the soil organic layer. In a recent review on mushroom allelopathy, Araya [16,17] proposed that the routes of release for allelochemicals from mushrooms were similar to those in plants. The allelopathic activity of mushrooms depends on hyphae biomass and on the amount/strength/variety of allelochemicals, in addition to the tolerance of affected organisms (e.g., plants or insects) [18]. Accordingly, using wild filamentous hyphae with fruiting bodies would be ideal for assessing the allelopathic potential of mushrooms. Because it is impossible to collect large amounts of wild filamentous hyphae for bioassay, the only available option is to use fruiting bodies, collectable aggregates of wild hyphae [16,17].
A simple and quick bioassay procedure is necessary to evaluate the allelopathic potential of a large number of mushroom samples. Several researchers have developed such methods to evaluate the allelopathic properties for individual plants/compounds [18,19,20,21,22,23,24,25,26]. These methods were designed based on the three main allelochemical release routes of plants: leaf litter leachates, roots exudates (in vitro and roots exudates in the soil), and volatiles. In the present study, we used the sandwich method to evaluate the allelopathic potential of the fruiting bodies of 289 macro-fungi from Japan [16,17,27]. Lettuce (Lactuca sativa var. Great Lakes 366) was used as a test plant to represent the seedling growth disturbance, due to the advantage of its susceptibility and uniform growth response to allelochemicals. Consequently, information on the inhibitory or stimulatory effects of chemicals eluted from mushroom fruiting bodies lead to further considerations about mushroom allelopathy in the forests of Japan. Thus, a presumption was made that mushrooms produced allelopathic compounds that affect a test plant directly. The intention of this research is to assess the allelopathic potential of mushrooms and to discuss the necessity of mushroom allelopathy as one of the important factors in forest ecosystems.

2. Materials and Methods

2.1. Fungal Collection

More than 800 kinds of mushroom fruiting bodies were collected from various geographical locations in 24 prefectures in Japan between May 2000 and August 2016 (Figure 1). Taxonomic identification was carried out by two of the authors (Ishizaki and Araya) through morphological examination (specimen numbers provided at supplementary data). Mushroom samples of 670 fruiting bodies among them were categorized into the 289 species that were used in the study. All the collected fruiting bodies were cleaned and lyophilized, then finely pulverized and bottled for storage in a dark freezer (Sanyo, BioMedical Freezer MDF-U536D, Osaka, Japan). Each year, a bioassay was conducted on the mushrooms collected in that year. All collected mushroom species were stored in the Natural Products Chemistry Laboratory, School of Agriculture, Meiji University.

2.2. Bioassay of Allelopathic Activity of Mushroom Fruiting Bodies Using the Modified Sandwich Method

Samples were screened using the modified sandwich method, which was developed in our previous studies [14,19]. In the sandwich method, 10 or 50 mg of plant material is placed in each well of a 6-well plastic multidish. For mushrooms, however, our previous study showed that 10 mg of dried material was more suitable due to the strength of the activity observed with 50 mg [16,17]. Despite the fact that 50 mg is the minimum amount for plant material, 10 mg of mushroom powder is almost the maximum amount, based on our knowledge of natural conditions as discussed above. Low-temperature gelling agar (0.75% w/v) was used as a growth medium (Nacalai Tesque, Kyoto, Japan; gelling temperature from 30 to 31 °C). The agar was autoclaved at 115 °C for 15 min and then cooled to 40 °C in a water bath. The mushroom powder (10 mg) was placed in each well, and then 5 ml of the agar was added using an auto-pipette (Gilson Co. Ltd, Villiers-le-Bel, France). If the samples floated on the agar, then they were submerged in the agar using micro-spatulas until the agar gelled. After the complete gelatinization of the agar layer (within 30–60 min at room temperature), another 5 mL of agar was added over the first layer in each well and left for 60 min to solidify. In this way, the lower agar layer contained the mushroom materials and was shielded by the second, pure agar layer. Lettuce (Lactuca sativa L. Great Lakes 366, Takii Seed Co. Ltd, Kyoto, Japan) was used as the test plant due to its germination reliability, rapid and uniform growth response, susceptibility to chemicals, and exogenous bioactive compounds [28]. Five lettuce seeds were placed on the surface of each agar-containing well of the plate. This allowed for adequate water content for growth and covered the whole area of each well with plant material with adequate distance for their growth. The multidishes were sealed with plastic tape to prevent dehydration and incubated (BIOTEC 300-L, Shimadzu Rika Institute Co. Ltd, Kyoto, Japan) for 72 h at 25 °C in the dark. The lengths of the radicles and hypocotyls were measured with 1 mm accuracy. Each experiment was replicated three times and the results presented are the mean of the results of these three replicates.

2.3. Statistics

The percentage of the radicle and hypocotyl growth ratio of the lettuce seedlings was calculated for each sample compared with the control by the following formula:
Growth   ratio ( % ) = 100 × ( average   of   sample   length / average   of   control   length )
To measure the growth ratio of each of the 289 mushroom species, averages were calculated within the same species samples in advance.
For the evaluation of allelopathic activity among individual samples, the concept of the “standard deviation variance” was applied [12,29] to show how much individuals can vary from total mean of our normal population. The mean (m) and standard deviation (σ) were calculated and the criterion of the standard deviation variance (SDV) was estimated to rank the species that exhibited significant effects. Criteria indices (*: m−σ, **: m−1.5σ, ***: m−2σ, and ****: m−2.5σ) indicate that the radicle and hypocotyl growth rate data can be combined to provide a unique index for ranking all mushrooms. The number of samples that regulated lettuce seedling growth was counted within the range of 10% regulation. In addition, correlation between growth average ratios of radicle and hypocotyl was analyzed for all 16 fungal orders collected, in parallel with their total average of growth regulation.

3. Results

A total of 670 mushroom fruiting bodies belonging to 289 species of 16 orders of macro-fungi were identified and screened for allelopathic effects on the growth of lettuce seedlings. The results of both lettuce radicle and hypocotyl growth conformed to normal distribution (radicle kurtosis = 1.69 and skewness = 1.05; hypocotyl kurtosis = 0.71 and skewness = 0.27), and it was observed that radicle elongation was affected by allelopathic compounds more than the hypocotyl (Figure 2). The radicle and hypocotyl growth percentages of lettuce seedlings were in the range of 2.8–131% and 11.4–147% of the control, respectively. A range of lettuce radicle elongation from 0 to 30% was observed in 30 species, from 30 to 50% in 125 species, from 50 to 70% in 90 species, from 70 to 90% in 27 species, and from 91–100% in eight species. The remaining eight species exhibited stimulation effects (101–150%), according to standard deviation variance (SDV) with 99% confidence (Figure 2a). In the case of lettuce hypocotyl elongation, a range of 0–30% was observed in just one species, 30–50% in 13 species, 50–70% in 42 species, 70–90% in 109 species, and 91–100% in 48 species. The remaining 75 species stimulated lettuce hypocotyl growth (101–150%) (Figure 2b).
As shown in Figure 2a, 163 mushrooms inhibited lettuce radicle elongation up to the average point of 41.1%, and 147 mushrooms inhibited lettuce hypocotyl growth to the average point of 76.8% (Figure 2b). Of the screened mushroom species, 74% inhibited lettuce radicle growth over 50% (Figure 2a). In addition, only 12% of the mushroom species in this study inhibited hypocotyl growth by 50% (Figure 2b). A previous study, which examined 81 species (including cultivated specimens), reported that approximately 80% of the mushrooms inhibited radicle growth by 50% at the same application rate, and almost all of the species examined inhibited lettuce hypocotyl growth at various ranges [30].
The correlation between radicle and hypocotyl growth, as illustrated in Figure 3, suggests that radicle growth was inhibited to a higher degree than hypocotyl growth. Moreover, the high coefficient of the correlation (r = 0.809) suggests that the inhibition of the growth of the radicle was more affected than the hypocotyl, which indicates that the radicle is more susceptible to this.
The standard deviation variance analysis suggested that the 54 species listed in Table 1 significantly inhibited both radicle and hypocotyl growth. With reference to radicle growth, Calocybe gambosa (2.8%), Cortinarius violaceus (4.3%), Xeromphalina tenuipes (5.1%), Clavaria miyabeana (7.6%), and Heimiella japonica (10.2%) showed the highest levels of inhibition of radicle elongation. Moreover, we observed that X. tenuipes (11.4%), Leucopaxillus septentrionalis (21.4%), Pholiota spumosa (25.1%), C. violaceus (27.4%), and Entoloma clypeatum (28.4%) exhibited the highest levels of hypocotyl elongation inhibition (Table 1). Conversely, the results based on the total estimation of criterion (99% confidence) showed that X. Tenuipes, radicle (R) = 5.1% and hypocotyl (H) = 11.4%, followed by C. violaceus, R = 4.3% and H = 27.4%, C. miyabeana, R = 7.6% and H = 38.8%, C. gambosa, R = 2.8% and H = 39.8%, E. clypeatum, R = 20.3% and H = 28.4%, P. Spumosa, R = 15.4% and H = 25.1%, and L. septentrionails, R = 14.8% and H = 21.4%, inhibited both radicle and hypocotyl elongation, similar to a previous study [31]. The strongest growth-inhibiting species belonged to Mycenaceae, Cortinariaceae, Clavariaceae, Lyophyllaceae, Entolomataceae, Strophariaceae, and Tricholomataceae of the phylum Basidiomycota (Table 1). Moreover, isolated bioactive compounds and the reported bioactivities of listed mushrooms are shown in Table 1.
Several species of tested mushrooms caused a slight stimulatory activity on the radicle and hypocotyl growth, which are plotted out of 100% as shown in Figure 3. Among these species, Ischnoderma resinosum and Exidia glandulosa stimulated the radicle and hypocotyl growth of lettuce to R = 130.6% and H = 142%, and R = 102.2% and H = 117%, respectively (Figure 3). This strong stimulatory activity of I. resinosum and E. glandulosa suggests that some allelochemical(s) can stimulate the growth of lettuce seedlings.
The SDV and mean with 99% confidence were calculated to assign various criteria (radicle growth and hypocotyl growth) to indicate significant inhibition levels among the mushroom species. Among the 289 species, the 54 species listed in Table 1 showed significant inhibition to merit criteria indices that indicate the level of growth inhibition.
The correlation between the hypocotyl and radicle growth regulation of lettuce by fungal orders is illustrated in Figure 4. Despite the varying number of collected mushrooms for each order, the order Corticiales exhibited the highest average growth inhibition activity (R = 24%; H = 66.2%) while Hymenochaetales presented the lowest growth inhibition activity (R = 65.7%; H = 99.3%). The order Agaricales had the highest number of species in this study (135), and four orders had only one species. The growth regulatory activity of mushroom orders on lettuce radicle and hypocotyl indicate that they follow a linear trend, suggesting that hypocotyl growth is less affected than radicle growth (Figure 4).
The 16 mushroom orders collected included 52 families. Boletaceae had the highest number of species (64 species), followed by Tricholomataceae (54 species), Strophariaceae (53 species), Polyporaceae (51 species), Amanitaceae (43 species), Agaricaceae (42 species), and Russulaceae (38 species) (supplementary data). There was no correlation, however, between mushroom families and their corresponding average of allelopathic activity.

4. Discussions

The sandwich method imitates allelopathy in natural conditions, i.e., the release of allelochemicals from litters; more so than using solvent extraction, because many of the less polar compounds present in extracts prepared using organic solvents are not released under natural conditions. Small pieces of herbaceous plant or tree leaves are used for the sandwich method, to mimic the fallen leaves and water-soluble contents that are extracted by rain without decomposition. Mushroom powder is easier to extract owing to the shorter existence time of fruiting bodies, the smaller size of mycelia than plant tissues, and the lack of hard tissue to decompose. Therefore, we consider that the result of the modified sandwich method using the powder of mushroom fruiting bodies reflects the true mushroom allelopathic potential. Normally distributed modified sandwich method data of 289 mushroom species showed that radicle growth was 41.1% and hypocotyl growth was 76.8% of their normal growth (Figure 2). This result indicates that mushrooms are remarkably stronger growth inhibitors than higher plants (R = 67.3%; H = 109%; growth average of 660 plants in literatures) [29,31,72]. In fact, plants generally have a larger aerial mass than mushrooms, and higher amounts of allelochemicals are produced in their reproductive organs than in mushroom fruiting bodies. However, the difference between the underground mass of plants and mushrooms is hard to measure, due to their different morphological states.
It is well known that some phytopathogenic fungi and fairy ring mushrooms produce specific phytotoxic secondary metabolites, such as brassicicolin, cyperin, imidazole-4-carboxyamide, and armillaridin; also, these metabolites can act as allelochemicals [73,74,75,76,77]. Although 119 species among the 289 screened species have been recorded as phytopathogenic (see the supplementary data) [75,76], only four species (C. gambosa, Bondarzewia mesenterica, Armillaria tabescens, and Phaeolus schweinitzii) among the 54 highly inhibitory species (Table 1) are phytopathogenic fungi. C. gambosa is a fairy ring fungus; it regulates the growth of neighboring plants and can be found under trees such as oak, beech, and conifer [35]. B. mesenterica is a strong saprotrophic decomposer and is phytopathogenic in wild forests in terms of its specific secondary metabolite, montadial A. Montadial A exhibits therapeutic cytotoxic activities against HL-60 cells [47] and is also a potential allelochemical. Many common trees and shrubs become infected by A. tabescens, which causes lethal root rot in coniferous forests as the most common phytopathogenic fungus [56,77,78]. Melleolides have been isolated from A. tabescens [56,57] and its analogues have been reported to have inhibitory effects on the growth of lettuce seedlings [5]. Melleolides may also act as allelochemicals. P. schweinitzii causes a major disease for old trees by limiting root growth [79] and may produce some root-specific phytotoxic compounds, although there are no reports of the allelopathic activity of hispidin and pinillidine, other isolates from P. schweinitzii [62,63], despite their potential plant growth-inhibiting effects. Approximately 40% of the 289 screened mushroom species were phytopathogenic, and these species may produce phytotoxins which may be allelopathic in certain ecosystems. This could be evidence to suggest that some phytotoxins from phytopathogenic mushrooms induce strong effects on their neighbor plants. To confirm this, further experiments testing a variety of plants should be carried out.
The results have shown that most of the wild mushrooms inhibited lettuce radicle and hypocotyl elongation, but in some cases, certain species stimulated lettuce growth. Radicle and hypocotyl growth percentages were in the range of 2.8–131% and 11.4–147%, respectively. In conclusion, radicle growth inhibition was stronger than hypocotyl growth inhibition. This was within expectations, since the radicle is more susceptible to allelochemicals due to its early emergence and direct exposure to the chemicals [80,81]. Moreover, the significant correlation between radicle and hypocotyl growth indicates that the difference between the inhibition of hypocotyl and radicle growth was induced by the mushrooms. Consequently, the modified sandwich method for the initial screening of allelopathic potential in mushrooms was found to be statistically reliable. The result will be applicable to discuss the influence of mushroom allelopathy in forest ecosystems. Further survey for evaluating the specific responses of forest plants to mushroom allelochemicals is necessary, despite the subsequent limitations of them (seed dormancy and uneven/varied germination). Another notable finding was that the most frequent mushroom orders did not show strong allelopathic activity compared with the rare orders. To clarify this finding, further experimental study should be carried out.

5. Conclusions

The modified sandwich method is applied as an accurate and inexpensive methodology for the initial screening of many kinds of mushroom samples, and our results conformed to normal distribution. Bioassay would also help overcome the current issue of applying naturally grown hyphae of wild mushrooms to studies of allelopathy. The screening results showed the presence of high levels of allelopathic effects on lettuce growth, suggesting that these mushrooms may exhibit such regulatory effects in their natural ecosystems. X. tenuipes and C. violaceus (both edible) were the top inhibiting species, and their potential allelochemicals could be exploited for sustainable weed management.
The average inhibition of lettuce seedling elongation by mushrooms in this study was higher than that reported for plants in other studies. Therefore, the results suggest that mushrooms play an important role in the regulation of forest ecosystems through allelopathy. In this manner, this report provides fundamental information on the allelopathic potentials of mushroom species in the wild for the analysis of natural ecosystems. Overall, our study reveals that allelopathy researchers should consider mushroom allelopathy as an important key to understanding ecological structures. Future research should focus on the isolation and identification of the specific allelochemicals involved in the most promising species of mushroom, as well as the mechanisms of their effects on target plant species.

Supplementary Materials

The supplementary data are available online at https://www.mdpi.com/1999-4907/9/12/773/s1.

Author Contributions

Current manuscript contains PhD work of A.O., H.A., and Y.F.; Conceptualization, A.O., H.A., K.S.A., H.M., T.I. and Y.F.; Formal analysis, A.O.; Investigation, A.O.; Methodology, H.A. and Y. F.; Resources, H.A. and T.I.; Software, A.O., K.S.A. and H.M.; Supervision, H.A. and Y.F.; Writing—original draft, A.O. and H.A.; Writing—review & editing, H.A., K.S.A., H.M., T.I. and Y.F. All authors were engaged in giving feedback on the manuscript and approved the final manuscript.

Funding

This study was supported by the grant-in-aid for Research on Agriculture and Food Science (25029AB) from the Ministry of Agriculture, Forestry, and Fisheries of Japan. JSPS KAKENHI Grant Number 26304024 also supported this work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Reigosa, M.J.; González, L. Forest ecosystems and allelopathy. In Allelopathy: A Physiological Process with Ecological Implications; Reigosa, M., Pedrol, N., González, L., Eds.; Springer: Dordrecht, The Netherlands, 2006; pp. 451–463. [Google Scholar]
  2. Blanco, J.A. The representation of allelopathy in ecosystem-level forest models. Ecol. Model. 2007, 209, 65–77. [Google Scholar] [CrossRef]
  3. Kumar, A.S.; Bais, H.P. Allelopathy and exotic plant invasion. In Plant Communication from an Ecological Perspective; Baluška, F., Ninkovic, V., Eds.; Springer: Berlin/Heidelberg, Germany, 2010; pp. 61–74. [Google Scholar]
  4. Williamson, G.B. Allelopathy, Koch’s postulates, and the neck riddle. In Perspectives on Plant Competition; Grace, J.B., Tilman, D., Eds.; Academic press, Inc.: San Diego, CA, USA; pp. 143–162.
  5. Choi, J.H.; Abe, N.; Tanaka, H.; Fushimi, K.; Nishina, Y.; Morita, A.; Kiriiwa, Y.; Motohashi, R.; Hashizume, D.; Koshino, H.; et al. Plant-growth regulator, imidazole-4-carboxamide, produced by the fairy ring forming fungus Lepista sordida. J. Agric. Food Chem. 2010, 58, 9956–9959. [Google Scholar] [CrossRef] [PubMed]
  6. Tobina, H.; Choi, J.H.; Asai, T.; Kiriiwa, Y.; Asakawa, T.; Kan, T.; Morita, A.; Kawagishi, H. 2-Azahypoxanthine and imidazole-4-carboxamide produced by the fairy-ring-forming fungus increase wheat yield. Field Crop. Res. 2014, 162, 6–11. [Google Scholar] [CrossRef] [Green Version]
  7. Badri, D.V.; Weir, T.L.; Van der Lelie, D.; Vivanco, J.M. Rhizosphere chemical dialogues: Plant-microbe interactions. Curr. Opin. Biotechol. 2009, 20, 642–650. [Google Scholar] [CrossRef]
  8. Biemelt, S.; Sonnewald, U. Plant-microbe interactions to probe regulation of plant carbon metabolism. J. Plant. Physiol. 2006, 163, 307–318. [Google Scholar] [CrossRef] [PubMed]
  9. Dangl, J.; Jones, J.D. Plant-microbe interactions affairs of the plant: Colonization, intolerance, exploitation and co-operation in plant-microbe interactions. Curr. Opin. Plant Biol. 1998, 1, 285–287. [Google Scholar] [CrossRef]
  10. Jonasson, S.; Castro, J.; Michelsen, A. Interactions between plants, litter and microbes in cycling of nitrogen and phosphorus in the arctic. Soil Biol. Biochem. 2006, 38, 526–532. [Google Scholar] [CrossRef]
  11. Brown, R.T. Influence of naturally occurring compounds on germination and growth of jack pine. Ecology 1967, 48, 542–546. [Google Scholar] [CrossRef]
  12. Wardle, D.A.; Karban, R.; Callaway, R.M. The ecosystem and evolutionary contexts of allelopathy. Trends Ecol. Evolut. 2011, 26, 655–662. [Google Scholar] [CrossRef] [Green Version]
  13. Wurzbacher, C.M.; Bärlocher, F.; Grossart, H.P. Fungi in lake ecosystems. Aquat. Microb. Ecol. 2010, 59, 125–149. [Google Scholar] [CrossRef] [Green Version]
  14. Fujii, Y.; Shibuya, T.; Nakatani, K.; Itani, T.; Hiradate, S.; Parvez, M.M. Assessment method for allelopathic effect from leaf litter leachates. Weed Biol. Manag. 2004, 4, 19–23. [Google Scholar] [CrossRef]
  15. Miller, R.M.; Fitzsimons, M.S. Fungal Growth in Soil. In Architecture and Biology of Soils: Life in Inner Space; Ritz, K., Young, I., Eds.; CABI: London, UK, 2011; p. 150. [Google Scholar]
  16. Araya, H. Allelochemicals of Mushrooms. In Recent Agrochemicals and Technical Papers (in Japanese); CMC publishing: Tokyo, Japan, 2017; pp. 568–577. [Google Scholar]
  17. Araya, H. Allelopathy of Mushrooms. In New Developments in Allelopathy Research; Price, J.E., Ed.; Nova Publisher: New York, NY, USA, 2015; pp. 1–14. [Google Scholar]
  18. Fujii, Y.; Pariasca, D.; Shibuya, T.; Yasuda, T.; Kahn, B.; Waller, G.R. Plant-box method: A specific biosassay to evaluate allelopathy through root exudates. In Allelopathy: New Concepts and Methodology; Fujii, Y., Hiradate, S., Eds.; Science Publisher: Enfield, NH, USA, 2007; pp. 39–56. [Google Scholar]
  19. Fujii, Y. Screening of allelopathic candidates by new specific discrimination, and assessment methods for allelopathy, and the identification of L-DOPA as the allelopathic substance from the most promising velvetbean (Mucuna pruriens). Bull. Natl. Inst. Agro-Environ. 1994, 10, 115–218. [Google Scholar]
  20. Fujii, Y.; Shibuya, T.; Yasuda, T. L-3,4-Dihydroxyphenylalanine as an allelochemical candidate from Mucuna pruriens (L.) DC. var. utilis. Agr. Biol. Chem. 1991, 55, 617–618. [Google Scholar] [CrossRef]
  21. Hiradate, S.; Morita, S.; Sugie, H.; Fujii, Y.; Harada, J. Phytotoxic cis-cinnamoyl glucosides from Spiraea thunbergii. Phytochemistry 2004, 65, 731–739. [Google Scholar] [CrossRef] [PubMed]
  22. Hirai, N.; Sakashita, S.I.; Sano, T.; Inoue, T.; Ohigashi, H.; Premasthira, C.U.; Asakawa, Y.; Harada, J.; Fujii, Y. Allelochemicals of the tropical weed Sphenoclea zeylanica. Phytochemistry 2000, 55, 131–140. [Google Scholar] [CrossRef]
  23. Iqbal, Z.; Nasir, H.; Hiradate, S.; Fujii, Y. Plant growth inhibitory activity of Lycoris radiata Herb. and the possible involvement of lycorine as an allelochemical. Weed Biol. Manag. 2006, 6, 221–227. [Google Scholar] [CrossRef]
  24. Kamo, T.; Hiradate, S.; Fujii, Y. First isolation of natural cyanamide as a possible allelochemical from hairy vetch Vicia villosa. J. Chem. Ecol. 2003, 29, 275–283. [Google Scholar] [CrossRef]
  25. Nakano, H.; Fujii, Y.; Yamada, K.; Kosemura, S.; Yamamura, S.; Hasegawa, K.; Suzuki, T. Isolation and identification of plant growth inhibitors as candidate(s) for allelopathic substance(s), from aqueous leachate from mesquite (Prosopis juliflora (Sw.) DC.) leaves. Plant Growth Regul. 2002, 37, 113–117. [Google Scholar] [CrossRef]
  26. Takemura, T.; Kamo, T.; Ismil, R.; Bakar, B.; Wasano, N.; Hiradate, S.; Fujii, Y. Plant growth inhibitor from the Malaysian medicinal plant Goniothalamus andersonii and related species. Nat. Prod. Commun. 2012, 7, 1197–1198. [Google Scholar]
  27. Araya, H. Allelopathic activities in litters of mushrooms. In New Discoveries in Agrochemicals; Clark, J.M., Ohkawa, H., Eds.; American Chemical Society: Washington, DC, USA, 2005; pp. 63–72. [Google Scholar]
  28. Fujii, Y.; Matsuyama, M.; Hiradate, S.; Shimozawa, H. Dish pack method: A new bioassay for volatile allelopathy. In Proceedings of the 4th World Congress on Allelopathy, Establishing the Scientific Base, Fourth World Congress on Allelopathy, Wagga Wagga, New South Wales, Australia, 21–26 August 2005; pp. 493–497. [Google Scholar]
  29. Fujii, Y.; Parvez, S.S.; Parvez, M.; Ohmae, Y.; Iida, O. Screening of 239 medicinal plant species for allelopathic activity using the sandwich method. Weed Biol. Manag. 2003, 3, 233–241. [Google Scholar] [CrossRef]
  30. Araya, H. Fruiting bodies of mushrooms as allelopathic plants. In Allelopathy: New Concepts and Methodology; Fujii, Y., Hiradate, S., Eds.; Science Publisher: Enfield, NH, USA, 2007; pp. 341–352. [Google Scholar]
  31. Morikawa, C.I.O.; Miyaura, R.; Tapiay-Figueroa, M.D.L.; Rengifo-Salgado, E.L.; Fujii, Y. Screening of 170 Peruvian plant species for allelopathic activity by using the sandwich method. Weed Biol. Manag. 2012, 12, 1–11. [Google Scholar] [CrossRef]
  32. Sari, M.; Prange, A.; Lelley, J.I.; Hambitzer, R. Screening of beta-glucan contents in commercially cultivated and wild growing mushrooms. Food Chem. 2017, 216, 45–51. [Google Scholar] [CrossRef] [PubMed]
  33. Spiteller, P.; Rüth, M.; Von Nussbaum, F.; Steglich, W. Detection of a 2,3-Aminomutase in the mushroom Cortinarius violaceus. Angew. Chem. 2000, 39, 2754–2756. [Google Scholar] [CrossRef]
  34. Ikeda, M.; Naganuma, Y.; Ohta, K.; Sassa, T.; Miura, Y. Isolation and identification of a plant-growth inhibitor, azetidine-2-carboxylic acid, from Clavaria miyabeana S. Ito and its occurrence in the family Clavariaceae. J. Agr. Chem. Soc. Jpn. 1977, 51, 519–522. [Google Scholar]
  35. Sitta, N.; Floriani, M. Nationalization and globalization trends in the wild mushroom commerce of Italy with emphasis on porcini (Boletus edulis and allied Species), Econ. Bot. 2008, 62, 307. [Google Scholar] [CrossRef]
  36. Clericuzio, M.; Tabasso, S.; Garbarino, J.A.; Piovano, M.; Cardile, V.; Russo, A.; Vidari, G. Non-Phenolic dicinnamamides from Pholiota Spumosa: Isolation, synthesis and antitumour activity. Eur. J. Org. Chem. 2007, 70, 137–139. [Google Scholar] [CrossRef]
  37. Barua, B.S.; Ohya, T.; Suzuki, A.; Fujimoto, H. Screening of the wild mushrooms producing antioxidants, Part-1. In Abstracts of Papers Presented at the Meeting of the Mycological Society of Japan, Proceedings of the 50th Anniversary of Annual Meeting for the Mycological Society of Japan; The Mycological Society of Japan: Tokyo, Japan, 2006. [Google Scholar] [CrossRef]
  38. Luo, H.; Liu, Y.; Fang, L.; Li, X.; Tang, N.; Zhang, K. Coprinus comatus damages nematode cuticles mechanically with spiny balls and produces potent toxins to immobilize nematodes. Appl. Environ. Microbiol. 2007, 73, 3916–3923. [Google Scholar] [CrossRef] [PubMed]
  39. Akiyama, H.; Toida, T.; Sakai, S.; Amakura, Y.; Kondo, K.; Sugita-Konishi, Y.; Maitani, T. Determination of cyanide and thiocyanate in Sugihiratake mushroom using HPLC method with fluorometric detection. J. Health Sci. 2006, 52, 73–77. [Google Scholar] [CrossRef]
  40. Wakimoto, T.; Asakawa, T.; Akahoshi, S.; Suzuki, T.; Nagai, K.; Kawagishi, H.; Kan, T. Proof of the existence of an unstable amino acid: Pleurocybellaziridine in Pleurocybella porrigens. Angew. Chem. 2011, 123, 1200–1202. [Google Scholar] [CrossRef]
  41. Kawagishi, H.; Miyazawa, T.; Kume, H.; Arimoto, Y.; Inakuma, T. Aldehyde dehydrogenase inhibitors from the mushroom Clitocybe clavipes. J. Nat. Prod. 2002, 65, 1712–1714. [Google Scholar] [CrossRef] [PubMed]
  42. Edwards, P.J. Effects of the fairy ring fungus Agaricus arvensis on nutrient availability in grassland. New Phytol. 1988, 110, 377–381. [Google Scholar] [CrossRef]
  43. Iwafuchi, Y.; Morita, T.; Kobayashi, H.; Kasuga, K.; Ito, K.; Nakagawa, O.; Kunisada, K.; Miyazaki, S.; Kamimura, A. Delayed onset acute renal failure associated with Amanita pseudoporphyria hongo ingestion. Internal. Med. 2003, 42, 78–81. [Google Scholar] [CrossRef]
  44. Endo, Y.; Minowa, A.; Kanamori, R.; Araya, H. A rare α-pyrone from bitter tooth mushroom, Sarcodon scabrosus (Fr.) Karst. Biochem. Syst. Ecol. 2012, 44, 286–288. [Google Scholar] [CrossRef]
  45. Hirota, M.; Morimura, K.; Shibata, H. Anti-inflammatory compounds from the bitter mushroom, Sarcodon scabrosus. Biosci. Biotechnol. Biochem. 2002, 66, 179–184. [Google Scholar] [CrossRef] [PubMed]
  46. Kim, W.G.; Kim, J.W.; Ryoo, I.J.; Kim, J.P.; Kim, Y.H.; Yoo, I.D. Boletunones A and B, highly functionalized novel sesquiterpenes from Boletus calopus. Org. Lett. 2004, 6, 823–826. [Google Scholar] [CrossRef] [PubMed]
  47. Sontag, B.; Arnold, N.; Steglich, W.; Anke, T. Montadial A, a cytotoxic metabolite from Bondarzewia montana. J. Nat. Prod. 1999, 62, 1425–1426. [Google Scholar] [CrossRef]
  48. Chung, K.S.; Lee, J.S.; Jo, M.J.; Lee, I.S. Studies on the hemolytic activities of Korean wild mushrooms (ii)-screening of 22 mushrooms including Laccaria vinaceoavellanea for their hemolytic activities, Korean J. Mycol. 2000, 28, 123–125. [Google Scholar]
  49. Ohta, T.; Matsuda, M.; Kobayashi, T.; Nagao, S.; Nozoe, S. Laccarin, A new alkaloid from the mushroom, Laccaria vinaceoavellanea. Heterocycles 1996, 43, 685–690. [Google Scholar] [CrossRef]
  50. Teichert, A.; Lübken, T.; Schmidt, J.; Kuhnt, C.; Huth, M.; Porzel, A.; Wessjohann, L.; Arnold, N. Determination of β-carboline alkaloids in fruiting bodies of Hygrophorus spp. by liquid chromatography/electrospray ionisation tandem mass spectrometry. Phytochem. Anal. 2008, 19, 335–341. [Google Scholar] [CrossRef]
  51. Michels, K.; Heinke, R.; Schöne, P.; Kuipers, O.P.; Arnold, N.; Wessjohann, L.A. A fluorescence-based bioassay for antibacterials and its application in screening natural product extracts. J. Antibiot. 2015, 68, 734. [Google Scholar] [CrossRef]
  52. Elmastas, M.; Isildak, O.; Turkekul, I.; Temur, N. Determination of antioxidant activity and antioxidant compounds in wild edible mushrooms. J. Food Compos. Anal. 2007, 20, 337–345. [Google Scholar] [CrossRef]
  53. Arnone, A.; Cardillo, R.; Di Modugno, V.; Nasini, G. Secondary mould metabolites. Part 29. Isolation and structure elucidation of candicansol, 3-epi-illudol and 1-O-acetyl-3-epi-illudol, novel sesquiterpenoids from Clitocybe candicans, and absolute configuration of 3-epi-illudol. J. Chem. Soc. Perkin Trans. 1 1989, 0, 1995–2000. [Google Scholar] [CrossRef]
  54. Chen, J.T.; Su, H.J.; Huang, J.W. Isolation and identification of secondary metabolites of Clitocybe nuda responsible for inhibition of zoospore germination of Phytophthora capsici. J. Agric. Food. Chem. 2012, 60, 7341–7344. [Google Scholar] [CrossRef] [PubMed]
  55. Jiang, M.Y.; Yang, X.L.; Fang, L.Z.; Zhang, L.; Dong, Z.J.; Liu, J.K. Purpuracolide: A new alliacane sesquiterpene from the basidiomycete Gomphus purpuraceus. J. Chem. Sci. 2008, 63, 1012–1014. [Google Scholar] [CrossRef]
  56. Donnelly, D.M.; Konishi, T.; Dunne, O.; Cremin, P. Sesquiterpene aryl esters from Armillaria tabescens. Phytochemistry 1997, 44, 1473–1478. [Google Scholar] [CrossRef]
  57. Herath, H.B.; Jacob, M.; Wilson, A.D.; Abbas, H.K.; Nanayakkara, N.D. New secondary metabolites from bioactive extracts of the fungus Armillaria tabescens. Nat. Prod. Res. 2013, 27, 1562–1568. [Google Scholar] [CrossRef]
  58. Mihail, J.D. Bioluminescence patterns among North American Armillaria species. Fungal Biol. 2015, 119, 528–537. [Google Scholar] [CrossRef]
  59. Kim, K.H.; Noh, H.J.; Choi, S.U.; Park, K.M.; Seok, S.J.; Lee, K.R. Lactarane sesquiterpenoids from Lactarius subvellereus and their cytotoxicity. Bioorg. Med. Chem. Lett. 2010, 20, 5385–5388. [Google Scholar] [CrossRef]
  60. Kerrigan, R.W. Agaricus subrufescens, a cultivated edible and medicinal mushroom, and its synonyms. Mycologia 2005, 97, 12–24. [Google Scholar] [CrossRef]
  61. Breene, W.M. Nutritional and medicinal value of specialty mushrooms. J. Food. Protect. 1990, 53, 883–894. [Google Scholar] [CrossRef]
  62. Han, J.J.; Bao, L.; He, L.W.; Zhang, X.Q.; Yang, X.L.; Li, S.J.; Yao, Y.J.; Liu, H.W. Phaeolschidins A-E, five hispidin derivatives with antioxidant activity from the fruiting body of Phaeolus schweinitzii collected in the Tibetan Plateau. J. Nat. Prod. 2013, 76, 1448–1453. [Google Scholar] [CrossRef] [PubMed]
  63. Smolskaitė, L.; Slapšytė, G.; Mierauskienė, J.; Dedonytė, V.; Venskutonis, P.R. Antioxidant and genotoxic properties of hispidin isolated from Phaeolus schweinitzii mushroom. Int. J. Med. Mushrooms 2017, 19, 967–980. [Google Scholar] [CrossRef] [PubMed]
  64. Vaskovsky, V.E.; Khotimchenko, S.V.; Boolugh, E.M. Distribution of diacylglycerotrimethylhomoserine and phosphatidylcholine in mushrooms. Phytochemistry 1998, 47, 755–760. [Google Scholar] [CrossRef]
  65. Veau, B.; Guillot, J.; Damez, M.; Dusser, M.; Konska, G.; Botton, B. Purification and characterization of an anti-(A+B) specific lectin from the mushroom Hygrophorus hypothejus. Biochim. Biophys. Acta: Gen. Subj. 1999, 1428, 39–44. [Google Scholar] [CrossRef]
  66. Tsuchihashi, H.; Yadomae, T.; Miyazaki, T. Isolation and characterization of an endo-β-D-glucuronidase from the fungus Kobayasia nipponica. J. Biochem. 1984, 96, 1799–1805. [Google Scholar] [CrossRef] [PubMed]
  67. Mihail, J.D.; Bruhn, J.N. Dynamics of bioluminescence by Armillaria gallica, A. mellea and A. tabescens. Mycologia 2007, 99, 341–350. [Google Scholar] [CrossRef]
  68. Valášková, V.; De Boer, W.; Gunnewiek, P.J.K.; Pospíšek, M.; Baldrian, P. Phylogenetic composition and properties of bacteria coexisting with the fungus Hypholoma fasciculare in decaying wood. ISME 2009, 3, 1218. [Google Scholar] [CrossRef]
  69. Jeon, S.M.; Wang, E.J.; Ka, K.H. Growth Characteristics and Extracellular Enzyme Activities of Pholiota spp. Mycol. Rep. Proc. 2015, 27, 106. [Google Scholar]
  70. Komatsu, N.; Sakai, S.; Saito, G.; Kikumoto, S.; Kimura, K.; Taito Co Ltd.; Kaken Kagaku KK. Treatment of Bacterial Infections with Glucan Compositions. U.S. Patent 3,943,247, 9 March 1976. [Google Scholar]
  71. Keishi, H.; Fuyuki, S.; Naganori, O.; Saori, T.; Kazuyuki, H. Stimulative effects of (22E,24R)-ergosta-7,22-diene-3β,5α,6β-triol from fruiting bodies of Tricholoma auratum, on a mouse osteoblastic cell line, MC3T3-E1, on a mouse osteoblastic cell line, mc3t3-e1. Biol. Pharm. Bull. 2002, 25, 1040–1044. [Google Scholar] [CrossRef]
  72. Appiah, K.S.; Li, Z.; Zeng, R.S.; Luo, S.; Oikawa, Y.; Fujii, Y. Determination of allelopathic potentials in plant species in Sino-Japanese floristic region by sandwich method and dish pack method. IJBAS 2015, 4, 381. [Google Scholar] [CrossRef] [Green Version]
  73. Möbius, N.; Hertweck, C. Fungal phytotoxins as mediators of virulence. Curr. Opin. Plant Biol. 2009, 12, 390–398. [Google Scholar] [CrossRef] [PubMed]
  74. Pedras, M.S.C.; Chumala, P.B.; Jin, W.; Islam, M.S.; Hauck, D.W. The phytopathogenic fungus Alternaria brassicicola: Phytotoxin production and phytoalexin elicitation. Phytochemistry 2009, 70, 394–402. [Google Scholar] [CrossRef] [PubMed]
  75. Hongo, K.; Ikeda, Y. New Version of Mushroom’s Encyclopedia; Hashimoto Shinpo-do: Tokyo, Japan, 2013; ISBN 978-4-89379-158-0. (In Japanese) [Google Scholar]
  76. Imazeki, R.; Otani, Y.; Hongo, T.; Izawa, M. Fungi of Japan; Yama-kei: Tokyo, Japan, 2011; ISBN 978-4-635-09044-5. (In Japanese) [Google Scholar]
  77. Thies, W.G.; Russell, K.W. Controlling root rots in coniferous forests of Northwestern North America. In Proceedings of the Sixth International Conference on Root and Butt Rots of Forest Trees, Melbourne, Victoria and Gympie, Queensland, Australia, 25–31 August 1983; pp. 379–386. [Google Scholar]
  78. Kobori, H.; Sekiya, A.; Suzuki, T.; Choi, J.H.; Hirai, H.; Kawagishi, H. Bioactive sesquiterpene aryl esters from the culture broth of Armillaria sp. J. Nat. Prod. 2014, 78, 163–167. [Google Scholar] [CrossRef] [PubMed]
  79. Gilbertson, R.L.; Ryvarden, L. North American Polypores, Volume 2; Fungiflora: Oslo, Norway, 1987; pp. 437–885. [Google Scholar]
  80. Leuschner, C.; Backes, K.; Hertel, D.; Schipka, F.; Schmitt, U.; Terborg, O.; Runge, M. Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. trees in dry and wet years. For. Ecol. Manag. 2001, 149, 33–46. [Google Scholar] [CrossRef]
  81. Munir, A.T.; Tawaha, A.R.M. Inhibitory effects of aqueous extracts of black mustard on germination and growth of lentil. Pak. J. Agron. 2002, 1, 28–30. [Google Scholar] [CrossRef]
Forests 09 00773 g001 550
Figure 1. Locations of sampling sites in Japan: 24 prefectures indicated by stars.
Figure 1. Locations of sampling sites in Japan: 24 prefectures indicated by stars.
Forests 09 00773 g001
Forests 09 00773 g002 550
Figure 2. Probability density of the allelopathic effect of the 289 mushroom species on lettuce (Lactuca sativa var. Great Lakes 366) radicle growth (a) and hypocotyl growth (b), with the accumulative distribution of the number of involved species also illustrated.
Figure 2. Probability density of the allelopathic effect of the 289 mushroom species on lettuce (Lactuca sativa var. Great Lakes 366) radicle growth (a) and hypocotyl growth (b), with the accumulative distribution of the number of involved species also illustrated.
Forests 09 00773 g002
Forests 09 00773 g003 550
Figure 3. Correlation between radicle and hypocotyl growth of lettuce.
Figure 3. Correlation between radicle and hypocotyl growth of lettuce.
Forests 09 00773 g003
Forests 09 00773 g004 550
Figure 4. Correlation of radical and hypocotyl growth regulation with fungal orders. The radius of each circle is an indicator of the frequency of screened species in that specific order. The total average is shown with a cross-hatched circle.
Figure 4. Correlation of radical and hypocotyl growth regulation with fungal orders. The radius of each circle is an indicator of the frequency of screened species in that specific order. The total average is shown with a cross-hatched circle.
Forests 09 00773 g004
Table
Table 1. Characteristics of 54 significant Japanese mushroom species ranked by criterion index.
Table 1. Characteristics of 54 significant Japanese mushroom species ranked by criterion index.
OrdersFamilySpeciesProp.Pthg.R. Grw.H. Grw.CriteriaBio. Act. & Bi. Com.
AgaricalesMycenaceaeXeromphalina tenuipesSapro.No5.111.4******NR
AgaricalesCortinariaceaeCortinarius violaceusMyco.No4.327.4*****Cysteine protease inhibitor, (R)-β-dopa, β-glucans [32,33]
AgaricalesClavariaceaeClavaria miyabeanaMyco./Sapro.NR7.638.8****L-azetidine-2-carboxylic acid [34]
AgaricalesLyophyllaceaeCalocybe gambosaSapro.Yes2.839.8****Fairy ring [35]
AgaricalesEntolomataceaeEntoloma clypeatumMyco.No20.328.4****NR
AgaricalesStrophariaceaePholiota spumosaSapro.No15.425.1****(R)-2-hydroxyputrescine dicinnamamide [36]
AgaricalesTricholomataceaeLeucopaxillus septentrionalisSapro.No14.821.4****Antibiotic activity (clitocine), antioxidant activity [37]
BoletalesBoletaceaeHeimiella japonicaMyco.No10.247.7***NR
AgaricalesCoprinaceaeCoprinus comatusSapro.No15.633.2***Fucogalactan, antimicrobial activity, nematophagous [38]
AgaricalesEntolomataceaeEntoloma abortivumPara./Sapro.No19.440.7***NR
AgaricalesEntolomataceaeEntoloma sarcopumMyco.No18.538.0***NR
AgaricalesMarasmiaceaePleurocybella porrigensSapro.No16.234.0***Aziridine, cyanide salt [39,40]
AgaricalesTricholomataceaeClitocybe clavipesSapro.No23.531.5***Acetaldehyde dehydrogenase inhibitor [41]
AgaricalesAgaricaceaeAgaricus arvensisSapro.No13.050.9**Fairy ring, sinapic acid [42]
AgaricalesAmanitaceaeAmanita pseudoporphyriaMyco.No15.851.3**Nephrotoxin [43]
AgaricalesAmanitaceaeAmanita sinensisMyco.No17.354.2**NR
ThelephoralesBankeraceaeSarcodon scabrosusMyco.No12.245.6**Neosarcodonin, 4-Methoxy-6-phenyl-2H-pyran-2-one [44,45]
BoletalesBoletaceaeBoletellus floriformisMyco.No21.147.4**NR
BoletalesSuillaceaeBoletinus palusterMyco.No21.053.9**Xerocomic acid, variegatic acid, variegatorubin [46]
BoletalesBoletaceaeBoletus quercinusMyco.No13.854.4**NR
BoletalesBoletaceaeXanthoconium affineMyco.No20.752.7**NR
RussulalesBondarzewiaceaeBondarzewia mesentericaSapro.Yes17.349.3**Montadial A [47]
AgaricalesHydnangiaceaeLaccaria vinaceoavellaneaMyco.No12.846.4**Hemolytic toxins, laccarin (I) [48,49]
AgaricalesHygrophoraceaeHygrophorus erubescens var. capreolariusMyco.No19.744.8**Harmane and norharmane [50]
AgaricalesHygrophoraceaeHygrophorus pudorinusMyco.No19.244.5**Antibacterial activity [51]
AgaricalesInocybaceaeInocybe luteaMyco.No18.148.3**NR
PolyporalesPolyporaceaePolyporus squamosusPara./Sapro.No17.749.0**Antioxidant and antimicrobial activity [52]
AgaricalesTricholomataceaeClitocybe candicansSapro.No21.047.5**Candicansol, epi-illudol and 1-O-acetyl-3-epi-illudol [53]
AgaricalesTricholomataceaeClitocybe nudaSapro.NR18.051.9**Antibacterial (2-methoxy-5- methyl-6-methoxy-methyl-p-benzoquinone, 6-hydroxy-2H-pyran-3-carbaldehyde and indole-3-carbaldehyde) [54]
AgaricalesTricholomataceaeTricholosporum porphyrophyllumSapro.NR15.247.0**NR
GomphalesGomphaceaeGomphus purpuraceusMyco.No29.637.1**Purpuracolide [55]
GomphalesGomphaceaeRamaria fennicaMyco.No44.339.5**NR
AgaricalesPhysalacriaceaeArmillaria tabescensSapro.Yes44.339.5**Bioluminescence,4-dehydro-14-hydroxy-dihydromelleolide,4-dehydro-dihydro-melleolide, 14-hydroxy-dihydromelleolide, 13-hydroxy-4-methoxy-melleolide and 5β,10α-dihydroxy-l-orsellinate-dihydromelleolide, emestrin-F, emestrin-G, 6-O-(4-O-methyl-β-d-glucopyranosyl)-8-hydroxy-2,7-dimethyl-4H-benzopyran-4-one, purpuracolide, and cephalosporolide-J [56,57,58]
AgaricalesAgaricaceaeLanopila nipponicaNRNR20.069.8*NR
AgaricalesAgaricaceaeLycoperdon pratenseSapro.No16.171.5*NR
AuricularialesAuriculariaceaeExidia uvapassaSapro.No21.165.7*NR
AgaricalesCortinariaceaeCortinarius caperatusMyco.No19.773.7*NR
AgaricalesPluteaceaePluteus leoninusSapro.No14.157.9*NR
PolyporalesPolyporaceaeMicroporus vernicipesSapro.No12.357.6*NR
RussulalesRussulaceaeLactarius subvellereusMyco.No17.060.1*Subvellerolactones [59]
AgaricalesTricholomataceaeLepista graveolensSapro.No11.956.0*NR
AgaricalesAgaricaceaeAgaricus subrutilescensSapro.No21.848.6*L-α-amino-γ-nitraminobutyric acid [60]
AuricularialesAuriculariaceaeAuricularia minorSapro.No29.148.3*Antitumor activity [61]
BoletalesBoletaceaeLeccinum versipelleMyco.No21.651.3*NR
PolyporalesFomitopsidaceaePhaeolus schweinitziiSapro.Yes33.044.3*Antitumor and radical-scavenging activity, Hispidin, pinillidine [62,63]
AgaricalesHygrophoraceaeHygrophorus speciosusMyco.No31.843.6*NR
AgaricalesHygrophoraceaeHygrophorus hypothejusMyco.No24.443.7*Anti-(A+B) blood type specific lectin, 1,2-diacylglycero-O-4’-(N,N,N-trimethyl) homoserine [64,65]
PhallalesPhallaceaeKobayasia nipponicaMyco.No22.751.2*β-Glucuronidase [66]
AgaricalesPhysalacriaceaeArmillaria gallicaSapro.No21.652.9*Bioluminescence [67]
RussulalesRussulaceaeRussula neoemeticaMyco.No23.944.1*NR
AgaricalesStrophariaceaeHypholoma fasciculareSapro.No28.946.7*Bactericidal effects [68]
AgaricalesStrophariaceaePholiota terrestrisSapro.No26.051.2*Highest cellulase and laccase activities among Pholiota genius [69]
AgaricalesTricholomataceaeMelanoleuca verrucipesSapro.No24.044.6*Glucans [70]
AgaricalesTricholomataceaeTricholoma auratumMyco.No30.945.4*(22E,24R)-Ergosta-7,22-diene-3β,5α,6β-triol [71]
Mean (m) 41.1 76.8
Standard deviation (σ) 19.7 22.3
m−σ (*) 21.4 54.5
m−1.5σ (**) 11.5 43.4
m−2σ (***) 1.69 32.2
m−2.5σ (****) 21.1
Bi. Com.: Bioactive compounds; Bio. Act.: Bioactivity; H. Grw.: Hypocotyl growth; Myco.: Mycorrhizal; Para.: Parasitic; Prop.: Properties; Pthg.: Phytopathogenecity; R. Grw.: Radicle growth; Sapro.: Saprotroph; NR: No records. Criteria indices (*: m−σ; **: m−1.5σ; ***: m−2σ; ****: m−2.5σ) indicate that the radicle and hypocotyl growth rate data can be combined to provide a unique index (i.e., X. tenuipes R= ** (m−1.5σ) and H= **** (m−2.5σ) combined to ******).

Share and Cite

MDPI and ACS Style

Osivand, A.; Araya, H.; Appiah, K.S.; Mardani, H.; Ishizaki, T.; Fujii, Y. Allelopathy of Wild Mushrooms—An Important Factor for Assessing Forest Ecosystems in Japan. Forests 2018, 9, 773. https://doi.org/10.3390/f9120773

AMA Style

Osivand A, Araya H, Appiah KS, Mardani H, Ishizaki T, Fujii Y. Allelopathy of Wild Mushrooms—An Important Factor for Assessing Forest Ecosystems in Japan. Forests. 2018; 9(12):773. https://doi.org/10.3390/f9120773

Chicago/Turabian Style

Osivand, Asma, Hiroshi Araya, Kwame S. Appiah, Hossein Mardani, Takayuki Ishizaki, and Yoshiharu Fujii. 2018. "Allelopathy of Wild Mushrooms—An Important Factor for Assessing Forest Ecosystems in Japan" Forests 9, no. 12: 773. https://doi.org/10.3390/f9120773

APA Style

Osivand, A., Araya, H., Appiah, K. S., Mardani, H., Ishizaki, T., & Fujii, Y. (2018). Allelopathy of Wild Mushrooms—An Important Factor for Assessing Forest Ecosystems in Japan. Forests, 9(12), 773. https://doi.org/10.3390/f9120773

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop