Abstract
Yellow chanterelles are among the most popular wild edible ectomycorrhizal mushrooms worldwide. The representative European golden chanterelle, Cantharellus cibarius, has only once been reported to fruit under greenhouse conditions, due to the difficulty of establishing pure culture. Recently, we developed a new technique for establishing a pure culture of a Japanese golden chanterelle (Cantharellus anzutake), and conducted in vitro ectomycorrhizal synthesis using established strains and Pinus densiflora. Acclimated pine mycorrhizal seedlings colonized with C. anzutake in a pot system under laboratory conditions produced small but distinct basidiomata with developed basidiospores. C. anzutake mycorrhizae were established on Quercus serrata seedlings by inoculation of mycorrhizal root tips of the fungus synthesized on P. densiflora. A scaled-up C. anzutake–host system in larger pots (4 L soil volume) exhibited repeated fruiting at 20–24 °C under continuous light illumination at 150 μmol m−2 s−1 during a 2-year incubation period. Therefore, a C. anzutake cultivation trial is practical under controlled environmental conditions.
Similar content being viewed by others
References
Agerer R (2006) Fungal relationships and structural identify of their ectomycorrhizae. Mycol Prog 5:67–107. https://doi.org/10.1007/s11557-006-0505-x
Arora D, Dunham SM (2008) A new, commercially valuable chanterelle species, Cantharellus californicus sp. nov., associated with live oak in California, USA. Econ Bot 62:376–391. https://doi.org/10.1007/s12231-008-9042-7
Buyck B, Kauff F, Eyssartier G, Couloux A, Hofstetter V (2014) A multilocus phylogeny for worldwide Cantharellus (Cantharellales, Agaricomycetidae). Fungal Divers 64:101–121. https://doi.org/10.1007/s13225-013-0272-3
Buyck B (2016) Editorial: towards completing the world inventory for Cantharellus. Cryptogam Mycol 37:255–258. https://doi.org/10.7872/crym/v37.iss3.2016.255
Corner EJH (1966) A monograph of cantharelloid fungi. Oxford University Press, London
Danell E (1994) Formation and growth of the ectomycorrhiza of Cantharellus cibarius Fr. Mycorrhiza 5:89–97. https://doi.org/10.1007/BF00202339
Danell E (1999) Chapter 10: Cantharellus. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi: key genera in profile. Springer, Berlin, pp 251–267
Danell E, Alstrom S, Ternstrom A (1993) Pseudomonas fluorescens in association with fruit bodies of the ectomycorrhizal mushroom Cantharellus cibarius. Mycol Res 97:1148–1152. https://doi.org/10.1016/S0953-7562(09)80519-4
Danell E, Camacho FJ (1997) Successful cultivation of the golden chanterelle. Nature 385:303. https://doi.org/10.1038/385303a0
Danell E, Fries N (1990) Methods for isolation of Cantharellus species, and the synthesis of ectomycorrhizae with Picea abies. Mycotaxon 38:141–148
Donofrio NM, Oh Y, Lundy R, Pan H, Brown DE, Jeong JS, Coughlan S, Mitchell TK, Dean RA (2006) Global gene expression during nitrogen starvation in the rice blast fungus, Magnaporthe grisea. Fungal Genet Biol 43:605–617. https://doi.org/10.1016/j.fgb.2006.03.005
Debaud JC, Gay G (1987) In vitro fruiting under controlled conditions of the ectomycorrhizal fungus Hebeloma cylindrosporum associated with Pinus pinaster. New Phytol 105:429–435. https://doi.org/10.1111/j.1469-8137.1987.tb00880.x
Eastwood DC, Herman B, Noble R, Dobrovin-Pennington A, Sreenivasaprasad S, Burton KS (2013) Environmental regulation of reproductive phase change in Agaricus bisporus by 1-octen-3-ol, temperature and CO2. Fungal Genet Biol 55:54–66. https://doi.org/10.1016/j.fgb.2013.01.001
Endo N, Kawamura F, Kitahara R, Sakuma D, Fukuda M, Yamada A (2014) Synthesis of Japanese Boletus edulis ectomycorrhizae with Japanese red pine. Mycoscience 55:405–416. https://doi.org/10.1016/j.myc.2013.11.008
Fries E (1979) Germination of spores of Cantharellus cibarius. Mycologia 71:216–219
Furukawa H, Masuno K, Takeuchi Y (2016) Forest management of matsutake productive sites for the optimization to global warming. Annu Rep Nagano Pref For Res Ctr 30:87–100
Hamada M (1953) Matsutake. Shizen 8:56–64
Hibbett DS, Bauer R, Binder M, Giachini AJ, Hosaka K, Justo A, Larsson E, Larsson KH, Lawrey JD, Miettinen O, Nagy L, Nilsson RH, Weiss M, Thorn RG (2014) Agaricomycetes. In: McLaughlin DJ, Spatafora JW (eds) Systematics and evolution, 2nd edn. The Mycota VII Part A, Springer Verlag, Berlin, pp 373–429
Imazeki R, Hongo T (1989) Colored illustrations of mushrooms of Japan, II. Hoikusha, Osaka
Kauserud H, Heegaard E, Büntgen U, Halvorsen R, Egli S, Senn-Irlet B, Krisai-Greilhuber I, Dämon W, Sparks T, Nordén J, Høiland K, Kirk P, Semenov M, Boddy L, Stenseth NC (2012) Warming-induced shift in European mushroom fruiting phenology. Proc Natl Acad Sci U S A 109:14488–14493. https://doi.org/10.1073/pnas.1200789109
Kauserud H, Stige LC, Vik JO, Økland RH, Høiland K, Stenseth NC (2008) Mushroom fruiting and climate change. Proc Natl Acad Sci U S A 105:3811–3814. https://doi.org/10.1073/pnas.0709037105
Kawamura S (1908) Some summer fungi of Suwa III. Bot Mag 22:409–415
Kawamura S (1955) Icons of Japanese fungi (vol. 4). Kazamashobo, Tokyo (in Japanese)
Kinugawa K (1963) Ecological studies on the development of fruit-body in Armillaria matsutake Ito et Imai analysis of growth curves. Bull Univ Osaka Pref Ser B 14:27–60
Kües U, Badalyan SM, Gieβler A, Dörne B (2016) Asexual sporulation in Agaricomycetes. In: Wendland J (ed) The Mycota I: growth, differentiation and sexuality, 3rd edn. Springer, Heidelberg, pp 269–328
Kumari D, Reddy MS, Upadhyay RC (2013) Diversity of cultivable bacteria associated with fruiting bodies of wild Himalayan Cantharellus spp. Ann Microbiol 63:845–853. https://doi.org/10.1007/s13213-012-0535-3
Miles PG, Chang S-T (2004) Mushrooms: cultivation, nutritional value, medicinal effect, and environmental impact. CRC Press, Boca Raton
Liu N, Ning G-A, Liu X-H, Feng X-X, Lu J-P, Mao L-J, Su Z-Z, Wang Y, Zhang C-L, Lina F-C (2016) An autophagy gene, HoATG5, is involved in sporulation, cell wall integrity and infection of wounded barley leaves. Microbiol Res 192:326–335. https://doi.org/10.1016/j.micres.2016.08.008
Ogawa M (1978) The biology of matsutake mushroom. Tsukiji Shokan, Tokyo (in Japanese)
Ogawa W, Endo N, Fukuda M, Yamada A (2018) Phylogenetic analyses of Japanese golden chanterelles and a new species description, Cantharellus anzutake sp. nov. Mycoscience 59:153–165. https://doi.org/10.1016/j.myc.2017.08.014
Ogawa W, Endo N, Takeda Y, Kodaira M, Fukuda M, Yamada A (2019) Efficient establishment of pure cultures of the yellow chanterelle, Cantharellus anzutake, from ectomycorrhizal root tips, and the morphological characteristics of ectomycorrhizae and cultured mycelium. Mycoscience 60:45–53. https://doi.org/10.1016/j.myc.2018.08.003
Ohta A (1994) Production of fruit-bodies of a mycorrhizal fungus, Lyophyllum shimeji, in pure culture. Mycoscience 35:147–151. https://doi.org/10.1007/BF02318492
Olariaga I, Moreno G, Manjón JL, Salcedo I, Hofstetter V, Rodríguez D, Buyck B (2016) Cantharellus (Cantharellales, Basidiomycota) revisited in Europe through a multigene phylogeny. Fungal Divers 83:263–292. https://doi.org/10.1007/s13225-016-0376-7
Palmer GE, Horton JS (2006) Mushrooms by magic: making connections between signal transduction and fruiting body development in the basidiomycete fungus Schizophyllum commune. FEMS Microbiol Lett 262:1–8. https://doi.org/10.1111/j.1574-6968.2006.00341.x
Persson O (1997) The chanterelle book. Ten Speed Press, Berkeley
Pilz D, Molina R, Mayo J (2006) Effects of thining young forests on chanterelle mushroom production. J For 104:9–14. https://doi.org/10.1093/jof/104.1.9
Pilz D, Norvell L, Danell E, Molina R (2003) Ecology and management of commercially harbested chanterelle mushrooms. Gen. Tech. Rep. PNW-GTR-576. U.S. Department of Agriculture, Forest Service, Pacific Norhtwest Research Station, Portland, p 83
Saito C, Ogawa W, Kobayashi H, Yamanaka T, Fukuda M, Yamada A (2018) In vitro ectomycorrhization of Tricholoma matsutake strains is differentially affected by soil type. Mycoscience 59:89–97. https://doi.org/10.1016/j.myc.2017.09.002
Sakamoto Y (2018) Influences of environmental factors on fruiting body induction, development and maturation in mushroom-forming fungi. Fungal Biol Rev 32:236–248. https://doi.org/10.1016/j.fbr.2018.02.003
Sharma R, Rajak RC, Pandey AK (2008) Growth response of Dendrocalamus seedlings by ioculation with ectomycorrhizal fungi. Middle-East J Sci Res 3:200–206
Sharma R, Rajak RC, Pandey AK (2010) Evidence of antagonistic interactions between rhizosphere and mycorrhizal fungi associated with Dendrocalamus strictus (bamboo). J Yeast Fungal Res 1:112–117
Sharma R, Rajak RC, Pandey AK (2011) Ectomycorrhiza like interaction between Cantharellus tropicalis and Dendrocalamus strictus. J Agric Technol 7:413–421
Skromne I, Sánchez O, Aguirre J (1995) Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. Microbiol 141:21–28. https://doi.org/10.1099/00221287-141-1-21
Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York
Straastma G, Konings RNH, van Griensven LJLD (1985) A strain collection of the mycorrhizal mushroom Cantharellus cibarius obtained by germination of spores and culture of fruit body tissue. Trans Br Mycol Soc 85:689–697
Vaario LM, Yang X, Yamada A (2017) Biogeography of the Japanese gourmet fungus, Tricholoma matsutake: a review of the distribution and functional ecology of matsutake. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis, Ecological studies (analysis and synthesis), vol, vol 230. Springer, Cham, pp 319–344. https://doi.org/10.1007/978-3-319-56363-3_15
Watling R (1997) The business of fructification. Nature 385:299–300. https://doi.org/10.1038/385299a0
Yamada A, Katsuya K (1995) Mycorrhizal association of isolates from sporocarps and ectomycorrhizas with Pinus densiflora seedlings. Mycoscience 36:315–323. https://doi.org/10.1007/BF02268607
Yamada A, Ogura T, Ohmasa M (2001) Cultivation of mushrooms of edible ectomycorrhizal fungi associated with Pinus densiflora by in vitro mycorrhizal synthesis. I. Primordium and basidiocarp formation in open-pot culture. Mycorrhiza 11:59–66. https://doi.org/10.1007/s005720000092
Zhang J, Ren A, Chen H, Zhao M, Shi L, Chen M, Wang H, Feng Z (2015) Transcriptome analysis and its application in identifying genes associated with fruiting body development in basidiomycete Hypsizygus marmoreus. PLoS One 10(4):e0123025. https://doi.org/10.1371/journal.pone.0123025
Acknowledgments
This study was supported in part by JSPS KAKENHI Grant Number 15H01751 from Japan Society for the Promotion of Science, and a general research grant from Institute for Fermentation, Osaka.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All experiments were performed in compliance with the current laws of Japan.
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Supplementary Fig. 1
Workflow from ectomycorrhizal synthesis in vitro to the scaled-up 4-L jar system. (PNG 184 kb)
Supplementary Fig. 2
Morphology and anatomy of Cantharellus anzutake ectomycorrhizae on Pinus densiflora in vitro. Strains EN-51 (a–c), EN-52 (d–f), EN-53 (g–i), EN-60 (j–l) and EN-61 (m–o). External morphology of ectomycorrhizal root tips (a, d, g, j, m), mantle outer layer (b, e, h, k, n), and sectioned root cortex showing Hartig net (c, f, i, l, o). Abbreviations: fungal mantle, fm; Hartig net, hn; tannin cell, tc; cortical cell, cc; endodermal cell, ec. Bars: 20 μm. (PNG 6144 kb)
Supplementary Fig. 3
The 1-L jar system of ectomycorrhizal seedlings colonized by Cantharellus anzutake. (a) A Pinus densiflora seedling colonized by C-2 (C-2-10), and (b) a Quercus serrata seedling colonized by EN-51 (EN-51-1Q). (c) Fruiting of EN-51 (EN-51Q). The 1-L jar with the oak seedling shoot was temporarily capped with another inverted jar to retain humidity. (d, e) Ectomycorrhizal root tips of EN-51 (EN-51Q) on the oak host: ectomycorrhizal development of the monopodial-pyramidal type on a long root tip (d), and on the lateral roots (e). (PNG 7195 kb)
ESM 1
(DOCX 16 kb)
Rights and permissions
About this article
Cite this article
Ogawa, W., Takeda, Y., Endo, N. et al. Repeated fruiting of Japanese golden chanterelle in pot culture with host seedlings. Mycorrhiza 29, 519–530 (2019). https://doi.org/10.1007/s00572-019-00908-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-019-00908-z