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Visualizing the spatial distribution of ustalic acid in the fruiting body of Tricholoma kakishimeji

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Abstract

Imaging mass spectrometry (IMS) was conducted for the first time using ustalic acid (UA) and the fruiting body of Tricholoma kakishimeji to localize mushroom toxins. The mushroom materials were systematically collected in Japan, and analysis of the cross sections of the materials at a resolution of 120 μm using matrix-assisted laser desorption/ionization mass spectrometry (MALDI–IMS) revealed the localization of UA and its biogenically related metabolites. MALDI–IMS confirmed that UA was predominantly located on the entire surface of the fruiting body and accumulated in higher amounts in younger fruiting bodies than in mature ones. UA is the first toxic secondary metabolite in the genus Tricholoma locally identified using IMS in mushrooms.

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References

  1. Aoki W, Endo N, Ushijima S, Nagai H, Ito T, Fukuda M, Yamada A (2021) Taxonomic revision of the Japanese Tricholoma ustale and closely related species based on molecular phylogenetic and morphological data. Mycoscience 62:307–321. https://doi.org/10.47371/mycosci.2021.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Yamaura Y (2013) Recent trends of mushroom poisoning in Japan. Chudoku Kenkyu 26:39–43

    PubMed  Google Scholar 

  3. Sano Y, Sayama K, Arimoto Y, Inakuma T, Kobayashi K, Koshino H, Kawagishi H (2002) Ustalic acid as a toxin and related compounds from the mushroom Tricholoma ustale. Chem Commun (Camb). https://doi.org/10.1039/b202607d

    Article  PubMed  Google Scholar 

  4. Sawayama Y, Tsujimoto T, Sugino K, Nishikawa T, Isobe M, Kawagishi H (2006) Syntheses of naturally occurring terphenyls and related compounds. Biosci Biotechnol Biochem 70:2998–3003. https://doi.org/10.1271/bbb.60389

    Article  CAS  PubMed  Google Scholar 

  5. Hayakawa I, Watanabe H, Kigoshi H (2008) Synthesis of ustalic acid, an inhibitor of Na+, K+-ATPase. Tetrahedron 64:5873–5877. https://doi.org/10.1016/j.tet.2008.04.051

    Article  CAS  Google Scholar 

  6. Ito T, Nagai H, Aoki W, Yamada A, Kawagishi H, Fukaya M, Konishi H (2021) Quantification of ustalic acid, a chemotaxonomic marker, in Tricholoma ustale using liquid chromatography-mass spectrometry. J Nat Med 75:688–691

    Article  CAS  PubMed  Google Scholar 

  7. Taira S, Ikeda R, Yokota N, Osaka I, Sakamoto M, Kato M, Sahashi Y (2010) Mass spectrometric imaging of ginsenosides localization in Panax ginseng root. Am J Chin Med 38:485–493. https://doi.org/10.1142/S0192415X10008007

    Article  CAS  PubMed  Google Scholar 

  8. He F, Huang Y-F, Dai W, Qu X-Y, Lu J-G, Lao C-C, Luo W-H, Sun D-M, Wei M, Xiao S-Y, Xie Y, Liu L, Zhou H (2022) The localization of the alkaloids in Coptis chinensis rhizome by time-of-flight secondary ion mass spectrometry. Front Plant Sci 13:1092643

    Article  PubMed  PubMed Central  Google Scholar 

  9. Taira S, Yamaguchi N, Morimoto S, Tatsuta Y, Katano H, Ichiyanagi Y, Tsuneyama K, Kikuchi K (2016) Liver disease risk of xenobiotics due to percutaneous absorption revealed by nano-paldi imaging mass spectrometry. Int J Recent Sci Res 7:12589–12592

    Google Scholar 

  10. Tang W, Zhang Y, Li P, Li B (2023) Evaluation of intestinal drug absorption and interaction using quadruple single-pass intestinal perfusion coupled with mass spectrometry imaging. Anal Chem 95:3218–3227

    Article  CAS  PubMed  Google Scholar 

  11. Taira S, Tatsuta Y, Katano H (2017) Localization analysis of natural toxin of Solanum tuberosum L via mass spectrometric imaging. J Cook Sci Japan 50:20–24. https://doi.org/10.11402/cookeryscience.50.20

    Article  Google Scholar 

  12. Taira S, Hashimoto M, Saito K, Shido O (2012) Visualization of decreased docosahexaenoic acid in the hippocampus of rats fed an n-3 fatty acid-deficient diet by imaging mass spectrometry. J Biophys Chem 3:221–226

    Article  Google Scholar 

  13. Zaima N, Goto-Inoue N, Hayasaka T, Setou M (2010) Application of imaging mass spectrometry for the analysis of Oryza sativa rice. Rapid Commun Mass Spectrom 24:2723–2729. https://doi.org/10.1002/rcm.4693

    Article  CAS  PubMed  Google Scholar 

  14. Taira S, Tokai M, Kaneko D, Katano H, Kawamura-Konishi Y (2015) Mass spectrometry imaging analysis of location of procymidone in cucumber samples. J Agric Food Chem 63:6109–6112. https://doi.org/10.1021/acs.jafc.5b00957

    Article  CAS  PubMed  Google Scholar 

  15. Shiono K, Hashizaki R, Nakanishi T, Sakai T, Yamamoto T, Ogata K, Harada KI, Ohtani H, Katano H, Taira S (2017) Multi-imaging of cytokinin and abscisic acid on the roots of rice (Oryza sativa) using matrix-assisted laser desorption/ionization mass spectrometry. J Agric Food Chem 65:7624–7628. https://doi.org/10.1021/acs.jafc.7b02255

    Article  CAS  PubMed  Google Scholar 

  16. Bhandari DR, Shen T, Rompp A, Zorn H, Spengler B (2014) Analysis of cyathane-type diterpenoids from Cyathus striatus and Hericium erinaceus by high-resolution MALDI MS imaging. Anal Bioanal Chem 406:695–704. https://doi.org/10.1007/s00216-013-7496-7

    Article  CAS  PubMed  Google Scholar 

  17. Huang M-Z, Cheng S-C, Jhang S-S, Chou C-C, Cheng C-N, Shiea J, Popov IA, Nikolaev EN (2012) Ambient molecular imaging of dry fungus surface by electrospray laser desorption ionization mass spectrometry. Int J Mass Spectrom 325:172–182. https://doi.org/10.1016/j.ijms.2012.06.015

    Article  CAS  Google Scholar 

  18. Wang H, Wang Y (2023) Matrix-assisted laser-desorption/ionization-mass spectrometric imaging of psilocybin and its analogues in psychedelic mushrooms using a cesium chloride-coated target plate. Anal Bioanal Chem 415:735–745. https://doi.org/10.1007/s00216-022-04467-9

    Article  CAS  PubMed  Google Scholar 

  19. Barbosa I, Domingues C, Ramos F, Barbosa RM (2023) Analytical methods for amatoxins: a comprehensive review. J Pharm Biomed Anal. https://doi.org/10.1016/j.jpba.2023.115421

    Article  PubMed  Google Scholar 

  20. Kawamoto T (2003) Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch Histol Cytol 66:123–143. https://doi.org/10.1679/aohc.66.123

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Professor Hirokazu Kawagishi (Shizuoka University) for providing the ustalic acid standard. We would like to thank Enago (https://www.enago.com/) for English language editing.

Funding

This work was supported by JSPS KAKENHI (Grant Number [23K06201]).

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Authors

Contributions

Collection and identification of T. kakishimeji, WA and AY; identification of ustalic acid, TI and MF; experiment regarding MALDI–IMS measurement, ST and TI; writing, TI; review and editing, HN, MF, and KR; and supervision, TI and AY. All authors have read and approved the published version of the manuscript.

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Correspondence to Tetsuro Ito or Akiyoshi Yamada.

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The authors have no competing interests to declare that are relevant to the content of this article.

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Ito, T., Taira, S., Aoki, W. et al. Visualizing the spatial distribution of ustalic acid in the fruiting body of Tricholoma kakishimeji. J Nat Med (2024). https://doi.org/10.1007/s11418-024-01823-0

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