Abstract
Tricholoma matsutake is an ectomycorrhizal basidiomycete that associates with Pinaceae in the Northern Hemisphere and produces prized “matsutake” mushrooms. We questioned whether the symbiont could associate with a birch that is an early-successional species in boreal, cool-temperate, or subalpine forests. In the present study, we demonstrated that T. matsutake can form typical ectomycorrhizas with Betula platyphylla var. japonica; the associations included a Hartig net and a thin but distinct fungal sheath, as well as the rhizospheric mycelial aggregate “shiro” that is required for fruiting in nature. The in vitro shiro also emitted a characteristic aroma. This is the first report of an ectomycorrhizal formation between T. matsutake and a deciduous broad-leaved tree in the boreal or cool-temperate zones that T. matsutake naturally inhabits.
References
Amaranthus MP, Pilz D, Moore A, Abbott R, Luoma D (2000) American matsutake (Tricholoma magnivelare) across spatial and temporal scales. USDA Forest Service Gen Tech Rep PSW-GTR-178
Duddridge JA (1986a) The development and ultrastructure of ectomycorrhizae III. Compatible and incompatible interactions between Suillus grevillei (Klotzsch) Sing. and 11 species of ectomycorrhizal hosts in vitro in the absence of exogenous carbohydrate. New Phytol 103:457–464
Duddridge JA (1986b) The development and ultrastructure of ectomycorrhizae IV. Compatible and incompatible interactions between Suillus grevillei (Klotzsch) Sing. and a number of ectomycorrhizal hosts in vitro in the presence of exogenous carbohydrate. New Phytol 103:465–471
Guerin-Laguette A, Shindo K, Matsushita N, Suzuki K, Lapeyrie F (2004) The mycorrhizal fungus Tricholoma matsutake stimulates Pinus densiflora seedling growth in vitro. Mycorrhiza 14:397–400
Guerin-Laguette A, Matsushita N, Lapeyrie F, Shindo K, Suzuki K (2005) Successful inoculation of mature pine with Tricholoma matsutake. Mycorrhiza 15:301–305
Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, London, pp 1–483
Hashimoto Y (1998) Ecological study of ectomycorrhizas of Betula platyphylla var. japonica. Thesis: United Graduate School of Agricultural Science, Gifu University.
Hosford D, Pilz D, Molina R, Amaranthus M (1997) Ecology and management of the commercially harvested American Matsutake mushrooms USDA Forest Service Gen Tech Rep PNW-GTR-412
Kobayashi H, Watahiki T, Kuramochi M, Onose K, Yamada Y (2007) Production of pine seedlings with shiro-like structure of the matsutake mushroom (Tricholoma matsutake (S. Ito et Imai) Sing.) in a large culture bottle. Mush Sci Tech 15:151–155 (in Japanese)
Massicotte HB, Peterson RL, Melville LH (1989) Hartig net structure ectomycorrhizae synthesized between Laccaria bicolor (Tricholomataceae) and two hosts: Betula alleghaniensis (Betulaceae) and Pinus resionsa (Pinaceae). Am J Bot 76:1654–1667
Massicotte HB, Peterson RL, Ackerley CA, Melville LH (1990) Structure and ontogeny of Betula alleghaniensis – Pisolithus tinctorius ectomycorrhizae. Can J Bot 68:579–593
Masui K (1927) A study of the ectotrophic mycorrhizas of woody plants. Mem Coll Sci, Kyoto Imper Univ 3:151–279
Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant–fungal process. Chapman and Hall Inc., NY, pp 357–423
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Murata H, Yamada A, Babasaki K (1999) Identification of repetitive sequences containing motifs of retrotransposons in the ectomycorrhizal basidiomycete Tricholoma matsutake. Mycologia 91:766–775
Murata H, Yamada A, Maruyama T, Endo N, Yamamoto K, Ohira T, Shimokawa T (2013) Root endophyte interaction between ectomycorrhizal basidiomycete Tricholoma matsutake and arbuscular mycorrhizal tree Cedrela odorata, allowing in vitro synthesis of rhizospheric “shiro”. Mycorrhiza 23:235–242
Murata H, Yamada A, Yokota S, Maruyama T, Endo N, Yamamoto K, Ohira T, Neda H (2014) Root endophyte symbiosis in vitro between the ectomycorrhizal basidiomycete Tricholoma matsutake and the arbuscular mycorrhizal plant Prunus speciosa. Mycorrhiza 24:315–321
Ogawa M (1975) Microbial ecology of mycorrhizal fungus, Tricholoma matsutake Ito et Imai (Sing.) in pine forest I – fungal colony (‘shiro’) of Tricholoma matsutake. Bull Gov For Exp Stat 272:79–121
Ogawa M (1977a) Microbial ecology of ‘shiro’ in Tricholoma matsutake (S. Ito et Imai) Sing. and its allied species. IV: Tricholoma matsutake and Tsuga diversifolia forests. Trans Myc Soc Jpn 18:20–33
Ogawa M (1977b) Microbial ecology of ‘shiro’ in Tricholoma matsutake (S. Ito et Imai) Sing. and its allied species. IV: Tricholoma matsutake and Tsuga sieboldii forests. Trans Myc Soc Jpn 18:34–46
Ogawa M (1978) The biology of matsutake.Tsukiji-shokan, Tokyo (in Japanese)
Sasse J (1998) The forests of Japan. Japan Forest Technical Association, Tokyo, pp 1–75
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press/Elsevier, London, pp 1–787
Vaario LM, Pennanen T, Sarjala T, Savonen EM, Heinonsalo J (2010) Ectomycorrhization of Tricholoma matsutake and two major conifers in Finland—an assessment of in vitro mycorrhiza formation. Mycorrhiza 20:511–518
Vaario LM, Fritze H, Spetz P, Savonen EM, Heinonsalo J, Hanajík P, Pennanen T (2011) Tricholoma matsutake dominates diverse microbial communities in different forest soils. Appl Environ Microbiol 77:8523–8531
Vaario LM, Heinonsalo J, Spetz P, Pennanen T, Heinonen J, Tervahauta A, Fritze H (2012) The ectomycorrhizal fungus Tricholoma matsutake is a facultative saprotroph in vitro. Mycorrhiza 22:409–418
Yamada A (1998a) Russula delica Fr. + Betula platyphylla Sukatchev var. japonicum Hara. (CDE16). In: Goodman DM, Durall DM, Trofymow JA, Berch SM (eds) A manual of concise descriptions of North American ectomycorrhizae, Fourth folio. Mycologue Publications, Sideny
Yamada A (1998b) Russula nigricans (Bull.:Fr.) Fr. + Betula platyphylla Sukatchev var. japonicum Hara. (CDE17). In: Goodman DM, Durall DM, Trofymow JA, Berch SM (eds) A manual of concise descriptions of North American ectomycorrhizae, Fourth folio. Mycologue Publications, Sideny
Yamada A, Kanekawa S, Ohmasa M (1999a) Ectomycorrhiza formation of Tricholoma matsutake on Pinus densiflora. Mycoscience 40:193–198
Yamada A, Maeda K, Ohmasa M (1999b) Ectomycorrhiza formation of Tricholoma matsutake isolates on seedlings of Pinus densiflora in vitro. Mycoscience 40:455–463
Yamada A, Maeda K, Kobayashi H, Murata H (2006) Ectomycorrhizal symbiosis in vitro between Tricholoma matsutake and Pinus densiflora seedlings that resembles naturally occurring ‘shiro’. Mycorrhiza 16:111–116
Yamada A, Kobayashi H, Murata H, Kalmiş E, Kalyoncu F, Fukuda M (2010) In vitro ectomycorrhizal specificity between the Asian red pine Pinus densiflora and Tricholoma matsutake and allied species from worldwide Pinaceae and Fagaceae forests. Mycorrhiza 20:333–339
Yamada A, Endo N, Murata H, Ohta A, Fukuda M (2014) Tricholoma matsutake Y1 strain associated with Pinus densiflora shows a gradient of in vitro ectomycorrhizal specificity with Pinaceae and oak hosts. Mycoscience 55:27–34
Yamanaka T, Konno M, Kawai M, Ohta A, Neda H, Terashima Y, Yamada A (2014) The host ranges of conifer-associated Tricholoma matsutake, Fagaceae-associated T. bakamatsutake and T. fulvocastaneum are wider in vitro than in nature. Mycologia 106:397–406
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This work was supported by grants from the Forestry and Forest Products Research Institute of Japan.
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Murata, H., Yamada, A., Maruyama, T. et al. Ectomycorrhizas in vitro between Tricholoma matsutake, a basidiomycete that associates with Pinaceae, and Betula platyphylla var. japonica, an early-successional birch species, in cool-temperate forests. Mycorrhiza 25, 237–241 (2015). https://doi.org/10.1007/s00572-014-0606-3
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DOI: https://doi.org/10.1007/s00572-014-0606-3