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Phylogenetic Relationships in Ganoderma Inferred from the Internal Transcribed Spacers and 25S Ribosomal DNA Sequences

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Phylogenetic Relationships in Ganoderma Inferred from the Internal Transcribed Spacers and 25S Ribosomal DNA Sequences Mycological Society of America Phylogenetic Relationships in Ganoderma Inferred from the Internal Transcribed Spacers and 25S Ribosomal DNA Sequences Author(s): Jean-Marc Moncalvo, Hsi-Hua Wang, Ruey-Shyang Hseu Source: Mycologia, Vol. 87, No. 2 (Mar. - Apr., 1995), pp. 223-238 Published by: Mycological Society of America Stable URL: http://www.jstor.org/stable/3760908 Accessed: 02/06/2009 05:58 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=mysa. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected]. Mycological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Mycologia. http://www.jstor.org Mycologia, 87(2), 1995, pp. 223-238. ? 1995, by The New York Botanical Garden, Bronx, NY 10458-5126 Phylogenetic relationships in Ganoderma inferred from the internal transcribed spacers and 25S ribosomal DNA sequences Jean-Marc Moncalvo' Key Words: Ganoderma,internal transcribed spac- Hsi-Hua Wang ers, nucleotide sequence, phylogeny, 25S ribosomal Ruey-Shyang Hseu RNA gene Applied MicrobiologyLaboratory, Department of Agricultural Chemistry,National Taiwan University, Taipei, Taiwan, Republic of China INTRODUCTION Ganoderma Karst. is a cosmopolitan genus of wood of Abstract: Over 250 species have been described in decaying polypore fungi economic importance. Sev- eral cause severe in Ganoderma.Species identification and species circum- species diseases plantations or in scription are often unclear and taxonomic segregation forests (Steyaert, 1967, 1972; Mahmood, 1971; Ross, Bakshi et Some of them of the genus remains controversial. In this study we 1976; al., 1976). have been shown to wood are sequenced the 5' half of the 25S ribosomal RNA gene selectively delignify and recognized as a source of and the internal transcribed spacers to determine ap- potentially important lignin-degrading and In propriate regions to i) discriminate between Ganod- enzymes (Otjen Blanchette, I987). the Orient, are used in folk to cure erma species and ii) infer taxonomic segregation of Ganodermaspecies medicine and strains are culti- Ganodermas. lato (Ganodermataceae) on a phyloge- various diseases, commercially vated for the of health tablets or drinks. netic basis. We studied 19 Ganodermaisolates repre- preparation The medicinal of Ganodermawere re- senting 14 species classified in 5 subgenera and sec- many benefits viewed and tions, one isolate of the related genus Amauroderma, by Jong Birmingham (1992). and one isolate of Fomitopsiswhich served as the out- The genus Ganodermawas established by Karsten group in parsimony analysis. Results showed that a (188i) for the laccate and stipitate white rot fungus transition bias was present in our data, and that rates Polyporus lucidus W. Curt. It was later amended by of nucleotide divergence in the different ribosomal Patouillard (1889) to include all polypores having dou- regions varied between lineages. Independent and ble-walled basidiospores. Ryvarden (i99I) noted that combined analyses of different data sets were per- the genus is presently in taxonomic chaos. Species formed and results were discussed. Nucleotide se- identification and species circumscription are often quences of the internal transcribed spacers, but not unclear, and the infrageneric segregation is contro- those of the coding regions, distinguished between versial (Steyaert, 1972, 1980; Corner, 1983; Zhao, 1989). most Ganodermaspecies, and indicated that isolates of Over 250 Ganodermaspecies have been described the G. tsugae group were misnamed. Phylogenetic worldwide, most of them from the tropics. Numerous analysis of the combined data sets of the divergent species have been described from pleomorphic char- domain D2 of the 25S ribosomal RNA gene and of acters. As a consequence, there are many synonyms the internal transcribed spacers indicated that sub- and several species complexes have been recognized genus Elfvingia was monophyletic, whereas sections (Steyaert, 1972, 1980; Bazzalo and Wright, 1982; Adas- Characoderma and Phaeonema were not. Combined data kaveg and Gilbertson, 1986; Yeh, 1990). For instance, from these regions is useful for infrageneric segre- Chen (1993) and Hseu (unpubl.) demonstrated in sev- gation of Ganodermaon a phylogenetic basis. Phylo- eral species that the shape of the basidiocarp was great- genetic analysis from data of the D2 region alone ly influenced by environmental factors. Also, Steyaert strongly supported Amaurodermaas a sister taxon of ('975) demonstrated in G. tornatum (Pers.) Bres. that Ganoderma.This suggested that the D2 region should basidiospore size varies with latitude and altitude, and be suitable for systematics at higher taxonomic ranks observed in G. lucidum (W. Curt.: Fr.) Karst. that con- in the Ganodermataceae. The low sequence variation text color was darker in collections from more south- observed in the 25S ribosomal gene within Ganoderma ern latitudes on the European continent (Steyaert, species suggested that the genus is young. I972). Patouillard (I889) divided the genus into two sec- Correspondingauthor. tions, sect. Ganodermaand sect. Amauroderma.The lat- Acceptedfor publicationDecember 27, 1994. ter was created to separate species characterized by 223 224 MYCOLOGIA subspherical or spherical basidiospores with the wall between biological species and to infer their phylo- uniformly thickened from those having basidiospores genetic relationships, while variation in the ITS regions truncated at the apex. Karsten (1889) established the was too low (Anderson and Stasovski, 1992). The IGR genus Elfvingia Karst. for nonlaccate Ganodermaspe- 1 region was useful for race identification in Puccinia cies, and Murrill (19o5a) raised AmaurodermaPat. to (Kim, 1992). The ITS regions were used for systematics generic rank. Murrill (I9o5b) created Tomophagusfor in Phytophthora (Lee and Taylor, 1992), in the Sclero- P. colossusFr. but the genus was considered a synonym tiniaceae (Carbone and Kohn, 1993), in boletes (Baura of Ganoderma by Furtado (i965), Steyaert (1972) and et al., 1992), in rusts (Zambino and Szabo, I993), and Ryvarden (I99i). Elfvingia was emended to include all in Talaromyces and Penicillium (LoBuglio et al., 1993). species lacking pilocystidia and reduced to subgeneric Divergent domains in the 25S rDNA were used for rank by Imazeki (1939), and was considered to be a species identification and phylogenetic studies in yeasts synonym of Ganodermaby Furtado (I965). Imazeki (Kurtzman, i992a, b), in Fusarium (Guadet et al., 1989), (1952) raised to generic level sect. Trachyderma Imaz. in Lyophyllum (Moncalvo et al., 1993) and in Lentinus (Imazeki, 1939), which was created to accommodate (Hibbett and Vilgalys, 1993). The latter study included G. tsunodae (Yasuda) Trott. Steyaert (1972) proposed G. lucidum and other polypores. three new genera, Haddowia, Humphreya and Mago- We sequenced the ITS regions and the 5' half of derna, for a mixture of Ganoderma and Amauroderma the 25S rDNA to determine appropriate regions to i) species. Later, he divided Ganodermainto four sub- discriminate between Ganodermaspecies and ii) infer genera and two sections on the basis of the cutis anat- segregation of Ganodermas. lato (Ganodermataceae omy (Steyaert, 1980), but Furtado (1965) and Corner Donk) on a phylogenetic basis. A comparison was also (1983) noted intermediacy between the described types made of rates and modes of evolution of the different of cutis and argued that alleged distinctions break rDNA regions studied, and phylograms produced from down in practice. Zhao et al. (I979) segregated subgen. independent and combined analyses of different data Ganodermaon the basis of context color. sets were critically examined. Besides morphological traits of fruitbodies, addi- tional taxonomic characters have been investigated for MATERIALS AND METHODS systematics of Ganoderma.Cultural studies were con- ducted by Nobles (1948), Stalpers (1978), Bazzalo and Organismsstudied. -The strains used in this study, their Wright (1982), Adaskaveg and Gilbertson (1986), Hseu origins, and their classification in Steyaert's (1980) or (1990), and Wang and Hua (1991). Isozyme electro- Zhao's (1989) system are presented in TABLE I. Isolate phoretic phenotypes were used by Hseu (1990). These CBS 428.84 was received from Centraalbureau voor methods produced new characters for studies at the Schimmelcultures (CBS), Baarn, Netherlands, as G. species level, but their use was not investigated at high- valesiacum Boud., but it was named G. tsugae Murr. by er taxonomic
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