Research Paper

Mycorrhizal fungi associated with Taiwanese Pyrola morrisonensis (Ericaceae) in a naturally regenerated forest

Yosuke Matsuda, Takashi Uesugi, Tsai-Wen Hsu and Chien-Fan Chen

Published on: 17 November 2017

DOI: 10.6165/tai.2017.62.399

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2017 vol.62 no.4 pp.399-406



Altschul, S.F., T.L. Madden, A.A. Sch?ffer, J. Zhang, Z. Zhang, W. Miller and D.J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids Res. 25(17): 3389-3402.
DOI: 10.1093/nar/25.17.3389View ArticleGoogle Scholar

Chou, W.-N. and Y.-Z. Wang. 2005. Nine species of Russula (Basidiomycotina) new to Taiwan. Taiwania 50(2): 93-100.
DOI: 10.6165/tai.2005.50(2).93View ArticleGoogle Scholar

Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST, Bioinformatics 26(19): 2460-2461.
DOI: 10.1093/bioinformatics/btq461View ArticleGoogle Scholar

Freudenstein, J.V. 1999. Relationships and character transformation in Pyroloideae (Ericaceae) based on ITS sequences, morphology, and development. Systematic Bot. 24(3): 398-408.
DOI: 10.2307/2419697View ArticleGoogle Scholar

Freudenstein J.V., B.B. Broe and E.R. Feldenkris. 2016. Phylogenetic relationships at the base of Ericaceae: implications for vegetative and mycorrhizal evolution. Taxon 65(4): 794-804.
DOI: 10.12705/654.7View ArticleGoogle Scholar

Gardes, M. and T.D. Bruns. 1993. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol. Ecol. 2(2): 113-118.
DOI: 10.1111/j.1365-294X.1993.tb00005.xView ArticleGoogle Scholar

Hashimoto, Y., S. Fukukawa, A. Kunishi, H. Suga, F. Richard, M. Sauve and M.A. Selosse. 2012. Mycoheterotrophic germination of Pyrola asarifolia dust seeds reveals convergences with germination in orchids. New Phytol. 195(3): 620-630.
DOI: 10.1111/j.1469-8137.2012.04174.xView ArticleGoogle Scholar

Hayata, B. 1908. Flora Montana Formosae. J. Coll. Sci. Imp. Univ. Tokyo 25: 155-156.

Huang, S., C.I Peng and H.C. Lee. 1987. Flavonoid analysis of Pyrola (Pyrolaceae) in Taiwan. Bot. Bull. Acad. Sin. 28: 283-287.

Hynson, N.A. and T.D. Bruns. 2009. Evidence of a myco-heterotroph in the plant family Ericaceae that lacks mycorrhizal specificity. Proc. R. Soc. Lond. B Biol. Sci. 276(1675): 4053-4059.
DOI: 10.1098/rspb.2009.1190View ArticleGoogle Scholar

Kato, K. and D.M. Standley. 2013. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 30(4): 772-780.
DOI: 10.1093/molbev/mst010View ArticleGoogle Scholar

Kinoshita, A., Y. Ogura-Tsujita, H. Umata, H. Sato, T. Hashimoto and T. Yukawa. 2016. How do fungal partners affect the evolution and habitat preferences of mycoheterotrophic plants? A case study in Gastrodia. Am. J. Bot. 103(2): 1-14.
DOI: 10.3732/ajb.1500082View ArticleGoogle Scholar

Kron, K.A., W.S. Judd, P.F. Stevens, D.M. Crayn, A.A. Anderberg, P.A. Gadek, C.J. Quinn and J.L. Luteyn. 2002. Phylogenetic classification of Ericaceae: molecular and morphological evidence. The Bot. Rev. 68(3): 335-423.
DOI: 10.1663/0006-8101(2002)068[0335:PCOEMA]2.0.CO;2View ArticleGoogle Scholar

Lallemand, F., M. Gaudeul, J. Lambourdi?re, Y. Matsuda, Y. Hashimoto and M.A. Selosse. 2016. The elusive predisposition to mycoheterotrophy in Ericaceae. New Phytol. 212(2): 314-319.
DOI: 10.1111/nph.14092View ArticleGoogle Scholar

Lallemand, F., ?. Puttsepp, M. Lang, A. Luud, P.E. Courty, C. Palancade and M.A. Selosse. 2017. Mixotrophy in Pyroleae (Ericaceae) from Estonian boreal forests does not vary with light or tissue age. Ann Bot. 120(3):361-371.
DOI: 10.1093/aob/mcx054View ArticleGoogle Scholar

Liu, Z.W., D.D. Jolles, J. Zhou, H. Peng and R.I. Milne. 2014. Multiple origins of circumboreal taxa in Pyrola (Ericaceae), a group with a Tertiary relict distribution. Annals Bot. 114(8): 1701-1709.
DOI: 10.1093/aob/mcu198View ArticleGoogle Scholar

Liu, Z.W., J. Zhou, E.D. Liu and H. Peng. 2010. A molecular phylogeny and a new classification of Pyrola (Pyroleae, Ericaceae). Taxon 59: 1690-1700.

Massicotte, H.B., L.H. Melville, L.E. Tackaberry and R.L. Peterson. 2008. A comparative study of mycorrhizas in several genera of Pyroleae (Ericaceae) from western Canada. Botany 86(6): 610-622.
DOI: 10.1139/B08-027View ArticleGoogle Scholar

Matsuda, Y., S. Shimizu, M. Mori, S. Ito and M.A. Selosse. 2012. Seasonal and environmental changes of mycorrhizal associations and heterotrophy levels in mixotrophic Pyrola japonica (Ericaceae) growing under different light environments. Am. J Bot. 99(7): 1177-1188.
DOI: 10.3732/ajb.1100546View ArticleGoogle Scholar

Obase, K. and Y. Matsuda. 2014. Culturable fungal endophytes in roots of Enkianthus campanulatus (Ericaceae). Mycorrhiza 24(8): 635-644.
DOI: 10.1007/s00572-014-0584-5View ArticleGoogle Scholar

Oksanen, J., F.G. Blanchet, R. Kindt, P. Legendre, P.R. Minchin, R.B. O'Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens and H. Wagner. 2013. Vegan: Community Ecology Package. R package version 2.0-10.

Peterson, R.L., H.B. Massicotte and L.H. Melville. 2004. Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa, Canada. R Core Team 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Robertson, D. C. and J. A. Robertson. 1985. Ultrastructural aspects of Pyrola mycorrhizae. Can. J. Bot. 63(6): 1089-1098.
DOI: 10.1139/b85-150View ArticleGoogle Scholar

Schloss, P.D., S.L. Westcott, T. Ryabin, J.R. Hall, M. Hartmann, E.B. Hollister, R.A. Lesniewski, B.B. Oakley, D.H. Parks, C.J. Robinson, J.W. Sahl, B. Stres, G.G. Thallinger, D.J. Van Horn and C.F. Weber. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microb. 75(23):7537-7541.
DOI: 10.1128/AEM.01541-09View ArticleGoogle Scholar

Selosse, M.A., F. Richard, X. He and S.W. Simard. 2006. Mycorrhizal networks: des liaisons dangereuses? Trends Ecol. Evol. 21(11): 621-628.
DOI: 10.1016/j.tree.2006.07.003View ArticleGoogle Scholar

Selosse M.A., M.F. Bocayuva, M.C.M. Kasuya and P.-E. Courty. 2016. Mixotrophy in mycorrhizal plants: extracting carbon from mycorrhizal networks. In Martin, F. (ed.), Molecular Mycorrhizal Symbiosis, 451-471. Springer, Berlin Heidelberg.
DOI: 10.1002/9781118951446.ch25View ArticleGoogle Scholar

Simard, S.W., K.J. Beiler, M.A. Bingham, J.R. Deslippe, L.J. Philip and P. Teste. 2012. Mycorrhizal networks: Mechanisms, ecology and modeling. Fungal Biol. Rev. 26(1): 39-60.
DOI: 10.1016/j.fbr.2012.01.001View ArticleGoogle Scholar

Smith, S.E. and D.J. Read. 2008. Mycorrhizal Symbiosis 3rd edition. Academic Press, London, UK.
DOI: 10.1016/B978-012370526-6.50002-7View ArticleGoogle Scholar

Takahashi, H. 1987. Pollen morphology and taxonomic position of two Taiwanese Pyrola: P. albo-reticulata Hayata and P. morrisonensis Hayata. J. Phytogeogr. Taxon. 35: 118-122.

Tamura, K., G. Stecher, D. Peterson, A. Filipski and S. Kumar. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30(12): 2725-2729.
DOI: 10.1093/molbev/mst197View ArticleGoogle Scholar

Taylor, D.L. and T.D. Bruns. 1999. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol. Ecol. 8(11): 1837-1850.
DOI: 10.1046/j.1365-294x.1999.00773.xView ArticleGoogle Scholar

Tedersoo, L., P. Pellet, U. K?ljalg and M.A. Selosse. 2007. Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151(2): 206-217.
DOI: 10.1007/s00442-006-0581-2View ArticleGoogle Scholar

Tedersoo, L., Jairus, T., Horton, B.M., Abarenkov, K., Suvi., T., Saar, I. and U. K?ljalg. 2008. Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol. 180(2): 479-490.
DOI: 10.1111/j.1469-8137.2008.02561.xView ArticleGoogle Scholar

Toftegaard, T., G.R. Iason, I.J. Alexander, S. Rosendahl and A.F.S. Taylor. 2010. The threatened plant intermediate wintergreen (Pyrola media) associates with a wide range of biotrophic fungi in native Scottish pine woods. Biodiver. Conserv. 19(14): 3963-3971.
DOI: 10.1007/s10531-010-9940-8View ArticleGoogle Scholar

Tschen, J.S.M., I.C. Ho, H.S. Hsu and E.F.C. Tschen. 2004. Distribution of macrofungi in the Quantaushi forest, a long-term ecological research site in Taiwan. Fung. Sci 19: 1-19.

Uesugi, T., M. Nakano, M.A. Selosse, K. Obase and Y. Matsuda. 2016. Pyrola japonica, a partially mycoheterotrophic Ericaceae, has mycorrhizal preference for russulacean fungi in central Japan. Mycorrhiza 26(8): 819-829.
DOI: 10.1007/s00572-016-0715-2View ArticleGoogle Scholar

van der Heijden, M.G.A., F. Martin, M.A. Selosse and I.R. Sanders. 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205(4): 1406-1423.
DOI: 10.1111/nph.13288View ArticleGoogle Scholar

Vincenot, L, L. Tedersoo, F. Richard, H. Horcine, U. K?ljalg and M.A. Selosse. 2008. Fungal associates of Pyrola rotundifolia, a mixotrophic Ericaceae, from two Estonian boreal forests. Mycorrhiza 19(1): 15-25.
DOI: 10.1007/s00572-008-0199-9View ArticleGoogle Scholar

White, T.J., T. Bruns, S. Lee and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA for phylogenetics. In: Innis, M. A. et al. (eds.), PCR protocols: a guide to methods and applications. 315-321. Academic Press, San Diego, USA.
DOI: 10.1016/B978-0-12-372180-8.50042-1View ArticleGoogle Scholar

Zimmer, K., N.A. Hynson, G. Gebauer, E.B. Allen, M.F. Allen and D.J. Read. 2007. Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytol. 175(1): 166-175.
DOI: 10.1111/j.1469-8137.2007.02065.xView ArticleGoogle Scholar