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Zotti M, Bonanomi G, Mazzoleni S. Fungal fairy rings: history, ecology, dynamics and engineering functions. IMA Fungus 2025; 16:e138320. [PMID: 40052080 PMCID: PMC11881004 DOI: 10.3897/imafungus.16.138320] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/01/2024] [Accepted: 01/04/2025] [Indexed: 03/09/2025] Open
Abstract
Fungal fairy rings (FFR) are fascinating natural phenomena that have intrigued people and scientists for centuries. These patterns, often represented by circular distributions of altered vegetation, are found in grasslands and forest habitats. Fairy rings occur when fungi grow radially in the soil, raising from a central point, progressively degrading organic matter and thus affecting vegetation. The observation of such spatial patterns allows mycologists to conduct an in-depth analysis of the role of fungi in ecosystems. This review presents the current knowledge and scientific advancement of the studies of FFRs. An historical appraisal from the most representative pioneer studies until recent works is presented in different scientific fields, including microbiology, chemistry, botany and ecology. Based on a deep analysis of bibliographic data, we synopsised different aspects of FFRs: i) history of studies, ii) taxonomy, iii) ecology (environmental conditions and biogeography), iv) classification of vegetation patterns, v) spatial dynamics, vi) role as ecosystem engineer (impact on soil chemistry, plants and microbiota). In conclusion, beside still open research areas requiring further investigation, a schematic functional model of fungal fairy rings is proposed, in which on one hand the dynamics of the fungal mycelium is explained by self-DNA accumulation and the build-up of autotoxicity. On the other hand, the effects of fungi on plants are related to the intermingled and differently spatially distributed effects of hydrophobicity, phytotoxicity and phytostimulation.
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Affiliation(s)
- Maurizio Zotti
- Department of Agricultural Sciences, University of Naples Federico II, Portici NA, via Università 100, Naples, ItalyUniversity of Naples Federico IIPorticiItaly
| | - Giuliano Bonanomi
- Department of Agricultural Sciences, University of Naples Federico II, Portici NA, via Università 100, Naples, ItalyUniversity of Naples Federico IIPorticiItaly
| | - Stefano Mazzoleni
- Department of Agricultural Sciences, University of Naples Federico II, Portici NA, via Università 100, Naples, ItalyUniversity of Naples Federico IIPorticiItaly
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Zineldeen DH, Mushtaq M, Haider KH. Cellular preconditioning and mesenchymal stem cell ferroptosis. World J Stem Cells 2024; 16:64-69. [PMID: 38455100 PMCID: PMC10915960 DOI: 10.4252/wjsc.v16.i2.64] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/11/2023] [Revised: 01/04/2024] [Accepted: 01/19/2024] [Indexed: 02/26/2024] Open
Abstract
In this editorial, we comment on the article published in the recent issue of the World Journal of Stem Cells. They focus on stem cell preconditioning to prevent ferroptosis by modulating the cystathionine γ-lyase/hydrogen sulfide (H2S) pathway as a novel approach to treat vascular disorders, particularly pulmonary hypertension. Preconditioned stem cells are gaining popularity in regenerative medicine due to their unique ability to survive by resisting the harsh, unfavorable microenvironment of the injured tissue. They also secrete various paracrine factors against apoptosis, necrosis, and ferroptosis to enhance cell survival. Ferroptosis, a regulated form of cell death characterized by iron accumulation and oxidative stress, has been implicated in various pathologies encompassing degenerative disorders to cancer. The lipid peroxidation cascade initiates and sustains ferroptosis, generating many reactive oxygen species that attack and damage multiple cellular structures. Understanding these intertwined mechanisms provides significant insights into developing therapeutic modalities for ferroptosis-related diseases. This editorial primarily discusses stem cell preconditioning in modulating ferroptosis, focusing on the cystathionase gamma/H2S ferroptosis pathway. Ferroptosis presents a significant challenge in mesenchymal stem cell (MSC)-based therapies; hence, the emerging role of H2S/cystathionase gamma/H2S signaling in abrogating ferroptosis provides a novel option for therapeutic intervention. Further research into understanding the precise mechanisms of H2S-mediated cytoprotection against ferroptosis is warranted to enhance the therapeutic potential of MSCs in clinical settings, particularly vascular disorders.
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Affiliation(s)
- Doaa Hussein Zineldeen
- Basic Sciences, Sulaiman AlRajhi University, Albukairiyah 52736, AlQaseem, Saudi Arabia
- Department of Medical Biochemistry and Molecular Biology, Faculty of Medicine, Tanta University, Tanta 6632110, Egypt
| | - Mazhar Mushtaq
- Basic Sciences, Sulaiman AlRajhi University, Albukairiyah 52736, AlQaseem, Saudi Arabia
| | - Khawaja Husnain Haider
- Basic Sciences, Sulaiman AlRajhi University, Albukairiyah 52736, AlQaseem, Saudi Arabia.
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Kotajima M, Choi JH, Suzuki H, Suzuki T, Wu J, Hirai H, Nelson DC, Ouchi H, Inai M, Dohra H, Kawagishi H. Identification of Biosynthetic and Metabolic Genes of 2-Azahypoxanthine in Lepista sordida Based on Transcriptomic Analysis. JOURNAL OF NATURAL PRODUCTS 2023; 86:710-718. [PMID: 36802627 DOI: 10.1021/acs.jnatprod.2c00789] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/18/2023]
Abstract
2-Azahypoxanthine was isolated from the fairy ring-forming fungus Lepista sordida as a fairy ring-inducing compound. 2-Azahypoxanthine has an unprecedented 1,2,3-triazine moiety, and its biosynthetic pathway is unknown. The biosynthetic genes for 2-azahypoxanthine formation in L. sordida were predicted by a differential gene expression analysis using MiSeq. The results revealed that several genes in the purine and histidine metabolic pathways and the arginine biosynthetic pathway are involved in the biosynthesis of 2-azahypoxanthine. Furthermore, nitric oxide (NO) was produced by recombinant NO synthase 5 (rNOS5), suggesting that NOS5 can be the enzyme involved in the formation of 1,2,3-triazine. The gene encoding hypoxanthine-guanine phosphoribosyltransferase (HGPRT), one of the major phosphoribosyltransferases of purine metabolism, increased when 2-azahypoxanthine content was the highest. Therefore, we hypothesized that HGPRT might catalyze a reversible reaction between 2-azahypoxanthine and 2-azahypoxanthine-ribonucleotide. We proved the endogenous existence of 2-azahypoxanthine-ribonucleotide in L. sordida mycelia by LC-MS/MS for the first time. Furthermore, it was shown that recombinant HGPRT catalyzed reversible interconversion between 2-azahypoxanthine and 2-azahypoxanthine-ribonucleotide. These findings demonstrate that HGPRT can be involved in the biosynthesis of 2-azahypoxanthine via 2-azahypoxanthine-ribonucleotide generated by NOS5.
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Affiliation(s)
| | | | | | - Tomohiro Suzuki
- Center for Bioscience Research and Education, Utsunomiya University, 350 mine-machi, Utsunomiya, Tochigi 321-8505, Japan
| | | | | | - David C Nelson
- Department of Botany and Plant Sciences, University of California, Riverside, California 92521, United States
| | - Hitoshi Ouchi
- School of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Makoto Inai
- School of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
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Li J, Guo L, Wilson GWT, Cobb AB, Wang K, Liu L, Zhao H, Huang D. Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands. BMC Ecol Evol 2022; 22:130. [PMID: 36335298 PMCID: PMC9636817 DOI: 10.1186/s12862-022-02082-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/27/2022] [Accepted: 10/19/2022] [Indexed: 11/06/2022] Open
Abstract
Background Fairy rings occur in diverse global biomes; however, there is a critical knowledge gap regarding drivers of fairy rings in grassland ecosystems. Grassland fairy rings are characterized belowground by an expanding mycelial front and aboveground by vigorous vegetation rings that develop concentrically with each growing season. We evaluated fairy ring dynamics in a field study conducted in semiarid grasslands to elucidate above- and belowground interactions driving distinct vegetation patterns. We followed this initial field investigation with a complementary greenhouse experiment, using soils collected from specific fairy ring zones (inside, ring-edge, outside) to examine plant-soil-microbial interactions under controlled conditions. We selected Leymus chinensis (a dominant grass) as our model plant species to assess the role of diverse fairy ring microbial communities on plant growth and nutrition. Results In our field study, plants on the ring-edge produced greater shoot biomass with higher concentrations of N and P, compared to plants inside the ring or adjacent (outside) controls. Soil microbial community biomarkers indicate shifts in relative microbial biomass as fairy rings expand. Inside the ring, plant roots showed greater damage from pathogenic fungi, compared to outside or ring-edge. Our greenhouse experiment confirmed that inoculation with live ring-edge soil generally promoted plant growth but decreased shoot P concentration. Inoculation with soil collected from inside the ring increased root pathogen infection and reduced shoot biomass. Conclusion We propose that soil microbial activity within ring-edges promotes plant growth via mobilization of plant-available P or directed stimulation. However, as the ring expands, L. chinensis at the leading edge may increase pathogen accumulation, resulting in reduced growth at the center of the ring in subsequent growing seasons. Our results provide new insights into the plant-soil-microbial dynamics of fairy rings in grasslands, helping to elucidate these mysterious vegetation patterns. Supplementary Information The online version contains supplementary material available at 10.1186/s12862-022-02082-x.
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Choi JH, Suzuki T, Ono A, Kotajima M, Tanaka Y, Suzuki T, Kawagishi H, Dohra H. The complete mitochondrial genome sequence of the fairy ring-forming fungus Lepista sordida. Mitochondrial DNA B Resour 2022; 7:712-714. [PMID: 35493712 PMCID: PMC9045758 DOI: 10.1080/23802359.2022.2067496] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022] Open
Abstract
Lepista sordida is a fairy ring-forming fungus that belongs to the family Tricholomataceae and is widely distributed in the Northern Hemisphere. Here, we report the complete mitochondrial genome sequence of L. sordida. The mitochondrial genome (57,375 bp) contained 20 protein-coding genes, 2 ribosomal RNA genes, and 26 transfer RNA genes. Phylogenetic analysis based on 14 conserved protein sequences from L. sordida and 15 related basidiomycetes showed that L. sordida was located on the outermost branch of the Tricholomataceae clade. This study is the first to report the complete mitochondrial genome sequence of a fairy ring-forming fungus belonging to the genus Lepista.
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Affiliation(s)
- Jae-Hoon Choi
- Research Institute of Green Science and Technology, Shizuoka University, Suruga-ku, Japan.,Graduate School of Science and Technology, Shizuoka University, Suruga-ku, Japan.,Graduate School of Integrated Science and Technology, Shizuoka University, Suruga-ku, Japan
| | - Tomohiro Suzuki
- Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya, Japan
| | - Akiko Ono
- Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya, Japan
| | - Mihaya Kotajima
- Graduate School of Science and Technology, Shizuoka University, Suruga-ku, Japan
| | - Yuki Tanaka
- Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya, Japan
| | - Toshiyuki Suzuki
- Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya, Japan
| | - Hirokazu Kawagishi
- Research Institute of Green Science and Technology, Shizuoka University, Suruga-ku, Japan.,Graduate School of Science and Technology, Shizuoka University, Suruga-ku, Japan.,Graduate School of Integrated Science and Technology, Shizuoka University, Suruga-ku, Japan
| | - Hideo Dohra
- Research Institute of Green Science and Technology, Shizuoka University, Suruga-ku, Japan.,Graduate School of Integrated Science and Technology, Shizuoka University, Suruga-ku, Japan
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Ito A, Choi JH, Yokoyama-Maruyama W, Kotajima M, Wu J, Suzuki T, Terashima Y, Suzuki H, Hirai H, Nelson DC, Tsunematsu Y, Watanabe K, Asakawa T, Ouchi H, Inai M, Dohra H, Kawagishi H. 1,2,3-Triazine formation mechanism of the fairy chemical 2-azahypoxanthine in the fairy ring-forming fungus Lepista sordida. Org Biomol Chem 2022; 20:2636-2642. [PMID: 35293930 DOI: 10.1039/d2ob00328g] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/21/2022]
Abstract
2-Azahypoxanthine (AHX) was first isolated from the culture broth of the fungus Lepista sordida as a fairy ring-inducing compound. It has since been found that a large number of plants and mushrooms produce AHX endogenously and that AHX has beneficial effects on plant growth. The AHX molecule has an unusual, nitrogen-rich 1,2,3-triazine moiety of unknown biosynthetic origin. Here, we establish the biosynthetic pathway for AHX formation in L. sordida. Our results reveal that the key nitrogen sources that are responsible for the 1,2,3-triazine formation are reactive nitrogen species (RNS), which are derived from nitric oxide (NO) produced by NO synthase (NOS). Furthermore, RNS are also involved in the biochemical conversion of 5-aminoimidazole-4-carboxamide-1-β-D-ribofuranosyl 5'-monophosphate (AICAR) to AHX-ribotide (AHXR), suggesting that a novel biosynthetic route that produces AHX exists in the fungus. These findings demonstrate a physiological role for NOS in AHX biosynthesis as well as in biosynthesis of other natural products containing a nitrogen-nitrogen bond.
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Affiliation(s)
- Akinobu Ito
- Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan. .,Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Jae-Hoon Choi
- Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan. .,Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan.,Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Waki Yokoyama-Maruyama
- Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan
| | - Mihaya Kotajima
- Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan.
| | - Jing Wu
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Tomohiro Suzuki
- Center for Bioscience Research and Education, Utsunomiya University, 350 Minemachi, Tochigi 321-8505, Japan
| | - Yurika Terashima
- Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan
| | - Hyogo Suzuki
- Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan
| | - Hirofumi Hirai
- Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan. .,Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan.,Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - David C Nelson
- Department of Botany and Plant Sciences, University of California, Riverside, California 92521, USA
| | - Yuta Tsunematsu
- Department of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Kenji Watanabe
- Department of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Tomohiro Asakawa
- Marine Science and Technology, Tokai University, 4-1-1 Kitakaname, Hiratsuka City, Kanagawa 259-1292, Japan
| | - Hitoshi Ouchi
- Department of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Makoto Inai
- Department of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Hideo Dohra
- Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan.,Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Hirokazu Kawagishi
- Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan. .,Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan.,Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
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7
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Duan M, Bau T. Grassland fairy rings of Leucocalocybe mongolica represent the center of a rich soil microbial community. Braz J Microbiol 2021; 52:1357-1369. [PMID: 33847922 DOI: 10.1007/s42770-021-00478-3] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/05/2020] [Accepted: 03/29/2021] [Indexed: 01/09/2023] Open
Abstract
BACKGROUND The ecological phenomenon of fungal fairy rings is usually found in grasslands and caused by the growth of specific fairy ring fungi in soil. The fairy rings are classified into three zones (DARK, DEAD, and OUT), and they have the potential to increase crop yield. Among these fairy rings, distinct characteristics of type I fairy rings can be seen in the rings formed by Leucocalocybe mongolica (LM). Our studies addressed changes in the soil microbial structure due to LM fairy rings to enhance understand of this ecological phenomenon. METHODS In the present study, we report the soil microbial analysis results (fungi and bacteria), including those of metabarcoding (16s rRNA, ITS), microbial quantity, and metagenomics surveys of soils collected from various fairy ring zones, of 6 LM fairy rings. All sampling sites cover the grasslands of Mongolian Plateau in China. RESULTS First, we found through metabarcoding surveys that the difference in microbial diversity is relatively less in bacteria and that the abundance of fairy ring fungi (LM) is relatively high in DEAD zones. We also identified eight bacterial and fungal families, including Sphingobacteriaceae and Sphingomonadaceae that were enriched within the soils of fairy ring zones. Second, we found that the abundance of soil bacteria in the DEAD zones is sharply increased along with the growth of fairy ring fungi (LM). Third, we found through shotgun sequencing that fairy ring-infected zones, DARK and DEAD, exhibit greater genetic diversity than OUT zones. Finally, we showed that the fairy ring ecosystem is the center for a rich grassland microbial community. CONCLUSIONS The reported data can improve our understanding of type I fairy rings and will be further insightful to the research on crop production.
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Affiliation(s)
- Mingzheng Duan
- College of Plant Protection, Jilin Agricultural University, Changchun, 130118, Jilin, China
- Key Laboratory of Edible Fungi Resources and Utilization (North), Ministry of Agriculture and Rural Affairs, Jilin Agricultural University, Changchun, 130118, Jilin, China
| | - Tolgor Bau
- College of Plant Protection, Jilin Agricultural University, Changchun, 130118, Jilin, China.
- Key Laboratory of Edible Fungi Resources and Utilization (North), Ministry of Agriculture and Rural Affairs, Jilin Agricultural University, Changchun, 130118, Jilin, China.
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Ouchi H, Namiki T, Iwamoto K, Matsuzaki N, Inai M, Kotajima M, Wu J, Choi JH, Kimura Y, Hirai H, Xie X, Kawagishi H, Kan T. S-Adenosylhomocysteine Analogue of a Fairy Chemical, Imidazole-4-carboxamide, as its Metabolite in Rice and Yeast and Synthetic Investigations of Related Compounds. JOURNAL OF NATURAL PRODUCTS 2021; 84:453-458. [PMID: 33480692 DOI: 10.1021/acs.jnatprod.0c01269] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/12/2023]
Abstract
During the course of our investigations of fairy chemicals (FCs), we found S-ICAr-H (8a), as a metabolite of imidazole-4-carboxamide (ICA) in rice and yeast (Saccharomyces cerevisiae). In order to determine its absolute configuration, an efficient synthetic method of 8a was developed. This synthetic strategy was applicable to the preparation of analogues of 8a that might be biologically very important, such as S-ICAr-M (9), S-AICAr-H (10), and S-AICAr-M (11).
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Affiliation(s)
- Hitoshi Ouchi
- School of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Takuya Namiki
- School of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Kenji Iwamoto
- School of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Nobuo Matsuzaki
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Makoto Inai
- School of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Mihaya Kotajima
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Jing Wu
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Jae-Hoon Choi
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Yoko Kimura
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Hirofumi Hirai
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Xiaonan Xie
- Center for Bioscience Research and Education, Utsunomiya University, 350 mine-machi, Utsunomiya, Tochigi 321-8505, Japan
| | - Hirokazu Kawagishi
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan
| | - Toshiyuki Kan
- School of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
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9
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Suzuki T. Genetic sequence analysis and characterization of bioactive compounds in mushroom-forming fungi. Biosci Biotechnol Biochem 2021; 85:8-12. [PMID: 33577662 DOI: 10.1093/bbb/zbaa067] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/04/2020] [Accepted: 10/26/2020] [Indexed: 11/12/2022]
Abstract
Mushroom-forming fungi produce unique bioactive compounds that have potential applications as medicines, supplements, and agrochemicals. Thus, it is necessary to clarify the biosynthetic pathways of these compounds using genome and transcriptome analyses. This review introduces some of our research on bioactive compounds isolated from mushrooms, as well as genetic analysis with next-generation sequencing.
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Affiliation(s)
- Tomohiro Suzuki
- Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya, Japan
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10
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Kawagishi H. Chemical studies on bioactive compounds related to higher fungi. Biosci Biotechnol Biochem 2021; 85:1-7. [PMID: 33577664 DOI: 10.1093/bbb/zbaa072] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/05/2020] [Accepted: 10/20/2020] [Indexed: 12/25/2022]
Abstract
Hericium erinaceus (Yamabushitake in Japan) is a well-known edible and medicinal mushroom. We discovered antidementia compounds, hericenones C to H, from the fruiting bodies and erinacine A to I from the cultured mycelia of the fungus. Based on the data of the compounds, several clinical experiments were performed using the fungus. "Fairy rings" is a phenomenon that turfgrass grows more prolific or inhibited than the surrounding area as a ring and then occasionally mushrooms develop on the ring. We found fairy-ring causing principles "fairy chemicals" and the biosynthetic routes of the compounds on the purine metabolic pathway in plants and mushrooms.
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Affiliation(s)
- Hirokazu Kawagishi
- Research Institute of Green Science and Technology, Shizuoka University, Suruga-ku, Shizuoka, Japan
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11
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Effects of imidazole-4-carboxamide and 2-azahypoxanthine on the growth and ectomycorrhizal colonization of Pinus densiflora seedlings inoculated with Tricholoma matsutake. MYCOSCIENCE 2020. [DOI: 10.1016/j.myc.2020.04.004] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/19/2022]
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12
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Ito A, Choi JH, Takemura H, Kotajima M, Wu J, Tokuyama S, Hirai H, Asakawa T, Ouchi H, Inai M, Kan T, Kawagishi H. Biosynthesis of the Fairy Chemicals, 2-Azahypoxanthine and Imidazole-4-carboxamide, in the Fairy Ring-Forming Fungus Lepista sordida. JOURNAL OF NATURAL PRODUCTS 2020; 83:2469-2476. [PMID: 32786881 DOI: 10.1021/acs.jnatprod.0c00394] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/11/2023]
Abstract
Fairy rings resulting from a fungus-plant interaction appear worldwide. 2-Azahypoxanthine (AHX) and imidazole-4-carboxamide (ICA) were first isolated from the culture broth of one of the fairy ring-forming fungi, Lepista sordida. Afterward, a common metabolite of AHX in plants, 2-aza-8-oxohypoxanthine (AOH), was found in AHX-treated rice. The biosynthetic pathway of the three compounds that are named as fairy chemicals (FCs) in plants has been partially elucidated; however, that in mushrooms remains unknown. In this study, it was revealed that the carbon skeletons of AHX and ICA were constructed from Gly in L. sordida mycelia and the fungus metabolized 5-aminoimidazole-4-carboxamide (AICA) to both of the compounds. These results indicated that FCs were biosynthesized by a diversion of the purine metabolic pathway in L. sordida mycelia, similar to that in plants. Furthermore, we showed that recombinant adenine phosphoribosyltransferase (APRT) catalyzed reversible interconversion not only between 5-aminoimidazole-4-carboxamide-1-β-d-ribofuranosyl 5'-monophosphate (AICAR) and AICA but also between ICA-ribotide (ICAR) and ICA. Furthermore, the presence of ICAR in L. sordida mycelia was proven for the first time by LC-MS/MS detection, and this study provided the first report that there was a novel metabolic pathway of ICA in which its ribotide was an intermediate in the fungus.
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Affiliation(s)
- Akinobu Ito
- Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan
| | | | - Hirohide Takemura
- Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan
| | | | | | | | | | - Tomohiro Asakawa
- Marine Science and Technology, Tokai University, 4-1-1 Kitakaname, Hiratsuka City, Kanagawa 259-1292, Japan
| | - Hitoshi Ouchi
- Department of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Makoto Inai
- Department of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Toshiyuki Kan
- Department of Pharmaceutical Sciences, University of Shizuoka, 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
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13
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Zotti M, De Filippis F, Cesarano G, Ercolini D, Tesei G, Allegrezza M, Giannino F, Mazzoleni S, Bonanomi G. One ring to rule them all: an ecosystem engineer fungus fosters plant and microbial diversity in a Mediterranean grassland. THE NEW PHYTOLOGIST 2020; 227:884-898. [PMID: 32266980 DOI: 10.1111/nph.16583] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/25/2019] [Accepted: 03/23/2020] [Indexed: 06/11/2023]
Abstract
Species coexistence in grasslands is regulated by several environmental factors and interactions with the soil microbial community. Here, the development of the Basidiomycetes fungus Agaricus arvensis, forming fairy rings, in a species-rich Mediterranean grassland, is described. Effects of the mycelial front on plants, fungi and bacteria were assessed by vegetation survey and next generation sequencing approaches. Our results showed a fungal-dependent shift in the community structure operated by a wave-like spread of fairy rings that decreased plant, fungal and bacterial diversity, indicating a detrimental effect of fairy rings on most species. The fairy rings induced successional processes in plants that enhanced the replacement of a community dominated by perennial plants with short-living and fast-growing plant species. In parallel, fungal and bacterial communities showed evident differences in species composition with several taxa associated within distinct sampling zone across the fairy rings. Notably, bacteria belonging to the Burkholderia genus and fungi of the genus Trichoderma increased in response to the advancing mycelium of A. arvensis. The profound changes in community composition and the overall increase in taxa diversity at ecosystemic scale suggest that fairy ring-forming fungi may act as ecosystem engineer species in Mediterranean grasslands.
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Affiliation(s)
- Maurizio Zotti
- Dipartimento di Agraria, Università di Napoli Federico II, Via Università, 100, 80055, Portici, Naples, Italy
| | - Francesca De Filippis
- Dipartimento di Agraria, Università di Napoli Federico II, Via Università, 100, 80055, Portici, Naples, Italy
- Task Force on Microbiome Studies, Università di Napoli Federico II, Corso Umberto I, 40, 80138, Naples, Italy
| | - Gaspare Cesarano
- Dipartimento di Agraria, Università di Napoli Federico II, Via Università, 100, 80055, Portici, Naples, Italy
| | - Danilo Ercolini
- Dipartimento di Agraria, Università di Napoli Federico II, Via Università, 100, 80055, Portici, Naples, Italy
- Task Force on Microbiome Studies, Università di Napoli Federico II, Corso Umberto I, 40, 80138, Naples, Italy
| | - Giulio Tesei
- Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università Politecnica delle Marche, via Brecce, Bianche, 60100, Ancona, Italy
| | - Marina Allegrezza
- Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università Politecnica delle Marche, via Brecce, Bianche, 60100, Ancona, Italy
| | - Francesco Giannino
- Dipartimento di Agraria, Università di Napoli Federico II, Via Università, 100, 80055, Portici, Naples, Italy
| | - Stefano Mazzoleni
- Dipartimento di Agraria, Università di Napoli Federico II, Via Università, 100, 80055, Portici, Naples, Italy
- Task Force on Microbiome Studies, Università di Napoli Federico II, Corso Umberto I, 40, 80138, Naples, Italy
| | - Giuliano Bonanomi
- Dipartimento di Agraria, Università di Napoli Federico II, Via Università, 100, 80055, Portici, Naples, Italy
- Task Force on Microbiome Studies, Università di Napoli Federico II, Corso Umberto I, 40, 80138, Naples, Italy
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14
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Choi JH, Matsuzaki N, Wu J, Kotajima M, Hirai H, Kondo M, Asakawa T, Inai M, Ouchi H, Kan T, Kawagishi H. Ribosides and Ribotide of a Fairy Chemical, Imidazole-4-carboxamide, as Its Metabolites in Rice. Org Lett 2019; 21:7841-7845. [PMID: 31518147 DOI: 10.1021/acs.orglett.9b02833] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
Abstract
The metabolism of imidazole-4-carboxamide (ICA) in plants has been unknown. Two metabolites (1 and 2) were isolated from ICA-treated rice, and their structures were determined by spectroscopic analysis including the single-crystal X-ray diffraction technique and synthesis. The ribotide of ICA (3), whose existence was predicted, was also synthesized and detected from the treated rice by LC-MS/MS. These results indicated that rice might interconvert ICA, 1, and 3 to regulate the biological activity.
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Affiliation(s)
- Jae-Hoon Choi
- Graduate School of Integrated Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan.,Research Institute of Green Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan
| | - Nobuo Matsuzaki
- Graduate School of Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan
| | - Jing Wu
- Research Institute of Green Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan
| | - Mihaya Kotajima
- Graduate School of Integrated Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan
| | - Hirofumi Hirai
- Graduate School of Integrated Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan.,Research Institute of Green Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan
| | - Mitsuru Kondo
- Research Institute of Green Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan
| | - Tomohiro Asakawa
- Tokai University Institute of Innovative Science and Technology , 4-1-1 Kitakaname , Hiratsuka City , Kanagawa 259-1292 , Japan
| | - Makoto Inai
- School of Pharmaceutical Sciences , University of Shizuoka , 52-1 Yada , Suruga-ku, Shizuoka 422-8526 , Japan
| | - Hitoshi Ouchi
- School of Pharmaceutical Sciences , University of Shizuoka , 52-1 Yada , Suruga-ku, Shizuoka 422-8526 , Japan
| | - Toshiyuki Kan
- School of Pharmaceutical Sciences , University of Shizuoka , 52-1 Yada , Suruga-ku, Shizuoka 422-8526 , Japan
| | - Hirokazu Kawagishi
- Graduate School of Integrated Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan.,Research Institute of Green Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan.,Graduate School of Science and Technology , Shizuoka University , 836 Ohya , Suruga-ku, Shizuoka 422-8529 , Japan
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15
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Takano T, Yamamoto N, Suzuki T, Dohra H, Choi JH, Terashima Y, Yokoyama K, Kawagishi H, Yano K. Genome sequence analysis of the fairy ring-forming fungus Lepista sordida and gene candidates for interaction with plants. Sci Rep 2019; 9:5888. [PMID: 30971747 PMCID: PMC6458111 DOI: 10.1038/s41598-019-42231-9] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/20/2018] [Accepted: 03/21/2019] [Indexed: 12/21/2022] Open
Abstract
Circular patterns called "fairy rings" in fields are a natural phenomenon that arises through the interaction between basidiomycete fungi and plants. Acceleration or inhibition of plant vegetative growth and the formation of mushroom fruiting bodies are both commonly observed when fairy rings form. The gene of an enzyme involved in the biosynthesis of these regulators was recently isolated in the fairy ring-forming fungus, Lepista sordida. To identify other genes involved in L. sordida fairy ring formation, we used previously generated sequence data to produce a more complete draft genome sequence for this species. Finally, we predicted the metabolic pathways of the plant growth regulators and 29 candidate enzyme-coding genes involved in fairy-ring formation based on gene annotations. Comparisons of protein coding genes among basidiomycete fungi revealed two nitric oxide synthase gene candidates that were uniquely encoded in genomes of fairy ring-forming fungi. These results provide a basis for the discovery of genes involved in fairy ring formation and for understanding the mechanisms involved in the interaction between fungi and plants. We also constructed a new web database F-RINGS ( http://bioinf.mind.meiji.ac.jp/f-rings/ ) to provide the comprehensive genomic information for L. sordida.
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Affiliation(s)
- Tomoyuki Takano
- Bioinformatics Laboratory, School of Agriculture, Meiji University, 1-1-1 Higashi-Mita, Kawasaki, 214-8571, Japan
| | - Naoki Yamamoto
- Bioinformatics Laboratory, School of Agriculture, Meiji University, 1-1-1 Higashi-Mita, Kawasaki, 214-8571, Japan
- Rice Research Institute, Sichuan Agricultural University, 211 Huiminglu, Wenjiang, Chengdu, China
| | - Tomohiro Suzuki
- Center for Bioscience Research and Education, Utsunomiya University, 350 Mine-machi, Utsunomiya, Tochigi, 321-8505, Japan
| | - Hideo Dohra
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan
| | - Jae-Hoon Choi
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan
| | - Yurika Terashima
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan
| | - Koji Yokoyama
- Bioinformatics Laboratory, School of Agriculture, Meiji University, 1-1-1 Higashi-Mita, Kawasaki, 214-8571, Japan
| | - Hirokazu Kawagishi
- Research Institute of Green Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan.
- Graduate School of Integrated Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan.
- Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan.
| | - Kentaro Yano
- Bioinformatics Laboratory, School of Agriculture, Meiji University, 1-1-1 Higashi-Mita, Kawasaki, 214-8571, Japan.
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16
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KAWAGISHI H. Are fairy chemicals a new family of plant hormones? PROCEEDINGS OF THE JAPAN ACADEMY. SERIES B, PHYSICAL AND BIOLOGICAL SCIENCES 2019; 95:29-38. [PMID: 30643094 PMCID: PMC6395780 DOI: 10.2183/pjab.95.003] [Citation(s) in RCA: 28] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/19/2018] [Accepted: 11/05/2018] [Indexed: 05/13/2023]
Abstract
2-Azahypoxanthine (AHX, 1) and imidazole-4-carboxamide (ICA, 2) were isolated from a fairy-ring-forming fungus Lepista sordida. AHX was converted into a metabolite 2-aza-8-oxo-hypoxanthine (AOH, 3) in plants. It was found out that these three compounds, named as fairy chemicals (FCs), endogenously exist in plants and are biosynthesized via a new purine metabolic pathway. FCs provided tolerance to the plants against various stresses and regulated the growth of all the plants. In addition, FCs increased the yield of rice, wheat, and other crops in the greenhouse and/or field experiments.
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Affiliation(s)
- Hirokazu KAWAGISHI
- Research Institute of Green Science and Technology, Shizuoka University, Shizuoka, Japan
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17
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Kawagishi H. Fairy chemicals - a candidate for a new family of plant hormones and possibility of practical use in agriculture. Biosci Biotechnol Biochem 2018. [PMID: 29513130 DOI: 10.1080/09168451.2018.1445523] [Citation(s) in RCA: 27] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/17/2022]
Abstract
2-Azahypoxanthine (AHX, 1) and imidazole-4-carboxamide (ICA, 2) were isolated from a fairy-ring forming fungus Lepista sordida. AHX was converted into a metabolite, 2-aza-8-oxohypoxanthine (AOH, 3), in plants. Afterward, it turned out that these three compounds, fairy chemicals (FSc), endogenously exist in plants and are biosynthesized via a new purine metabolic pathway. Furthermore, FCs increased the yields of rice, wheat and other crops in the filled experiments.
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Affiliation(s)
- Hirokazu Kawagishi
- Research Institute of Green Science and Technology, Shizuoka University, Shizuoka, Japan
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18
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Abstract
Abstract
Fungi including mushrooms have been proved to be an important biosource of numerous metabolites having a huge variety of chemical structures and diverse bioactivities. Metabolites of mushrooms are of remarkable importance as new lead compounds for medicine and agrochemicals. This review presents some of our studies on biologically functional molecules purified from mushroom-forming fungi; (1) endoplasmic reticulum stress suppressor, (2) osteoclast-forming suppressing compounds, (3) plant growth regulators.
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Affiliation(s)
- Jae-Hoon Choi
- College of Agriculture, Academic Institute, Shizuoka University, Shizuoka, Japan
- Research Institute of Green Science and Technology, Shizuoka University, Shizuoka, Japan
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19
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Choi JH, Wu J, Sawada A, Takeda S, Takemura H, Yogosawa K, Hirai H, Kondo M, Sugimoto K, Asakawa T, Inai M, Kan T, Kawagishi H. N-Glucosides of Fairy Chemicals, 2-Azahypoxanthine and 2-Aza-8-oxohypoxanthine, in Rice. Org Lett 2017; 20:312-314. [PMID: 29235343 DOI: 10.1021/acs.orglett.7b03736] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
Abstract
Plant growth stimulators, 2-azahypoxanthine (AHX) and 2-aza-8-oxohypoxanthine (AOH), were isolated from the fairy-ring-forming fungus, Lepista sordida, and AHX-treated rice, respectively. Further metabolites of AHX were detected in AHX-treated rice by HPLC, and the metabolites 1-4 were isolated from the rice. The structures of 1-4 were determined by spectroscopic analysis and synthesis. Compounds 1-4 exhibited no significant activity against rice, indicating that rice regulates the activity of AHX and AOH by converting them into their glucosides.
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Affiliation(s)
| | | | | | | | | | | | | | | | - Kunihisa Sugimoto
- Research & Utilization Division, Japan Synchrotron Radiation Research Institute , 1-1-1 Koto, Sayo-cho, Sayo-gun, Hyogo 679-5198, Japan
| | - Tomohiro Asakawa
- Tokai University Institute of Innovative Science and Technology , 4-1-1 Kitakaname, Hiratsuka City, Kanagawa 259-1292, Japan
| | - Makoto Inai
- School of Pharmaceutical Sciences, University of Shizuoka , 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
| | - Toshiyuki Kan
- School of Pharmaceutical Sciences, University of Shizuoka , 52-1 Yada, Suruga-ku, Shizuoka 422-8526, Japan
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20
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Davison EK, Sperry J. Natural Products with Heteroatom-Rich Ring Systems. JOURNAL OF NATURAL PRODUCTS 2017; 80:3060-3079. [PMID: 29135244 DOI: 10.1021/acs.jnatprod.7b00575] [Citation(s) in RCA: 57] [Impact Index Per Article: 7.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/07/2023]
Abstract
This review focuses on all known natural products that contain a "heteroatom-rich" ring system, specifically a five-, six- or seven-membered ring that contains three or more heteroatoms. The isolation and biological activity of these natural products is discussed, along with the biosynthetic processes that Nature employs to assemble these rare heterocyclic frameworks.
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Affiliation(s)
- Emma K Davison
- School of Chemical Sciences, University of Auckland , 23 Symonds Street, Auckland 1142, New Zealand
| | - Jonathan Sperry
- School of Chemical Sciences, University of Auckland , 23 Symonds Street, Auckland 1142, New Zealand
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