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Phylogeny and a new species of Sparassis (Polyporales, Basidiomycota): evidence from mitochondrial atp6, nuclear rDNA and rpb2 genes

     Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China

Zheng Wang ¹
Manfred Binder
David S. Hibbett

     Department of Biology, Clark University, 950 Main Street, Worcester, Massachusetts 01610

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS TAXONOMY PHYLOGENETIC ANALYSES DISCUSSION LITERATURE CITED

 

Three nuclear genes, lsu-rDNA (encoding nuclear large subunit rDNA), ITS (encoding the rDNA internal transcribed spacers and 5.8 S rDNA) and rpb2 (encoding the second largest subunit of RNA polymerase II), and the mitochondrial gene atp6 (encoding the sixth subunit of ATP synthase), were sequenced from all recognized Sparassis lineages. Sparassis latifolia sp. nov. from boreal coniferous forests in China is described based on morphological, ecological, geographical and molecular data. The nuclear gene phylogeny strongly supported groups corresponding to morphological differences, geographic distribution and host shifts among species that produce clamp connections, such as S. crispa from Europe, S. radicata from western North America and S. latifolia from Asia. The atp6 phylogeny however showed no divergence among these three species. For clampless Sparassis species, such as S. spathulata from eastern North America, S. brevipes and a new species from Europe, the atp6 phylogeny was congruent with the nuclear gene phylogeny. Sparassis cystidiosa is basal in the nuclear tree but sister to S. brevipes-S. spathulata clade in the ATP6 tree. The differences between the phylogenetic inferences from the atp6 gene and those from nuclear genes within Sparassis species are discussed.

Key words: clamp connections, mating tests, mitochondrial inheritance, sexual compatibility

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS TAXONOMY PHYLOGENETIC ANALYSES DISCUSSION LITERATURE CITED

 
The taxonomy and systematics of cauliflower fungi, species of Sparassis Fr., recently have received much attention (Blanco-Dios et al unpublished, Desjardin et al 2004, Wang et al 2004). Sparassis species have a bipolar mating system and produce a brown rot on conifers and Fagales. This is a derived wood decay mode in the Polyporales, which otherwise is dominated by white rot fungi (Hibbett and Donoghue 2001). Seven clades representing widely recognized species in Sparassis were reported based on molecular and morphological data (Desjardin et al 2004, Wang et al 2004). Presence of clamp connections is variable among Sparassis species, as well as among tissue in the basidiocarps of some species. In S. brevipes Krombh. and S. spathulata (Schwein.) Fr. no clamp connections are produced in the context, although clamp connections may be found in subhymenium and at the base of basidia. Species in four other clades produce clamp connections, including S. cystidiosa Desjardin and Zheng Wang from Thailand, which appears to be the sister group to all other Sparassis lineages, S. radicata Weir from western North America, S. crispa (Wulfen) Fr. from Europe and S. cf. crispa from Asia. Two collections from Spain with few clamp connections in the subhymenium represent a putatively new species, provisionally named S. "miniensis" and might be closely related to S. brevipes from northern Europe based on a rDNA phylogeny (Blanco-Dios et al pers. comm.).

Asian collections identified as S. crispa are morphologically different from S. crispa in Europe, and the Asian S. cf. crispa clade is strongly supported by molecular data. Wang et al (2004) did not describe these Asian collections as new, in part because appropriate materials for designating a type specimen were not available.

Mating studies (Martin and Gilbertson 1976) have cast doubts on the biological boundaries between S. crispa and S. radicata. Martin and Gilbertson (1976) crossed dikaryotic isolates of S. crispa from Europe and Japan with monokaryotic isolates of S. radicata from North America. The resulting Di-Mon mycelia produced clamp connections but did not produce fruiting bodies or basidia. Based on these results Martin and Gilbertson (1976) suggested that S. crispa and S. radicata were conspecific. They confirmed that S. radicata is heterothallic, that two S. radicata isolates exhibited a bipolar mating type and that matings between the two isolates were compatible. This was interpreted as evidence of multiple alleles for incompatibility in the S. radicata population (Martin and Gilbertson 1976). The eastern North American S. spathulata (S. crispa from southeastern north American in Martin and Gilbertson 1976), which produces no clamp connections in the context, produced basidiospores but no clamp connections in dikaryotic culture. However no mating studies with single spore isolates of S. spathulata were performed (Martin and Gilbertson 1976).

It is difficult to apply the biological species concept to fungi because little is known about the mating behavior of fungi in the field. Dikaryons produced by crossing monokaryotic isolates in the lab could fail to produce functional basidiospores for many reasons. Mating type genes regulate sexual compatibility and reproduction in fungi. Mating incompatibility inhibits crosses between closely related isolates of similar mating types. Some basidiomycetes possess complicated genetic systems that control the crossing from the very beginning of anastomosis between compatible hyphae to the production of fruiting bodies. For example more than 20 000 mating types can be formed in Schizophyllum commune Fr. because of the tremendous number of specificities generated by the subloci of two unlinked mating loci (Kronstad and Staben 1997). In the case of Sparassis no basidiospores were observed in Di-Mon matings within clamp producing species. This could indicate incompatibility among these fungi. However failure to produce fruiting bodies also could be a result of culture conditions or other factors not connected to genetic incompatibility.

It has been demonstrated that mitochondria do not migrate along with nuclei in sexual crosses in some basidiomycetes, although recombination between different mtDNAs still may occur in some cases (Baptista-Ferreita et al 1983, Hintz et al 1988, May and Taylor 1988). In Armillaria and Neurospora species both parental mitochondrial types are present in mycelia soon after mating but only one mitochondrial type becomes dominant during subsequent vegetative growth (Smith et al 1990, Lee and Taylor 1993). Homogenization of mitochondrial populations after mating also has been observed in Di-Mon pairings of Pleurotus ostreatus (Jacq. ex Fr.) Kummer, with mitochondria from the monokaryotic donor taking over the whole mycelium (Fischer and Wolfrath 1997). Thus the evidence to date suggests that mitochondria are uniparentally inherited in fungi.

Sequences of fungal mitochondrial rDNA (mt-lsu and mt-ssu) have been used for population studies and higher-level phylogenetic studies (e.g. Binder and Hibbett 2002, Lumbsch et al 2005). However the utility of mitochondrial rDNA is limited by high substitution rates in variable regions, the variable size of introns and the relatively small number of conserved regions that can be aligned across distantly related taxa (Hibbett and Donoghue 1995, Kretzer and Bruns 1999, Wang et al 2004, Lutzoni et al 2004). Few mt-lsu rDNA sequences have been generated from Sparassis species because of difficulties in primer design. A more promising candidate to trace mitochondrial inheritance is the mitochondrial gene atp6. The atp6 gene codes subunit 6 in a F₀·F₁-H⁺-ATP synthase, which is the main enzyme responsible for producing ATP in aerobic cells (Vinogradov 1999). Primers are available from the study of Kretzer and Bruns (1999), which suggested that phylogenetic inferences from mt-lsu and atp6 sequences are congruent and the combination of both genes increases support for the key clades in Boletales. A phylogeny of the genus Agaricus Fr. based on atp6 sequences suggested that variation within the atp6 genes was sufficient for studying species level relationships but was inadequate for lower level relationships (Robison et al 2001). In this study we discuss relationships among Sparassis species based on a combined nuclear gene phylogeny (nuclear large subunit rDNA, ITS, rpb2) with data drawn from Wang et al (2004) and comparative analyses using atp6.

	MATERIALS AND METHODS

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Morphological studies.— – Materials are deposited at the Herbarium of the Institute of Applied Ecology, Chinese Academy of Sciences (IFP). For comparison seven specimens from the Botanical Museum of the University of Helsinki (H) were studied. The microscopic procedures followed those described by Dai (1999). These abbreviations are used: L = mean spore length (arithmetical mean of all spores), W = mean spore width (arithmetical mean of all spores), Q = mean L/W ratios (quotient of the mean spore length and the mean spore width), n = number of spores measured from given number of specimens. In presenting the variation in the size of spores 5% of the measurements were excluded from each end of the range and are given in parentheses. The abbreviation IKI stands for Melzer’s reagent (IKI–means inamyloid), KOH for 5% potassium hydroxide and CB for cotton blue (CB+ means cyanophilous).

Molecular techniques.— – DNA was isolated from dried herbarium material following standard protocols as described in Wang et al (2004). Sequence data of lsu-rDNA, rpb2, and ITS generated in Wang et al (2004) and Blanco-Dios et al (generated by ZW at Clark University unpublished) were used in this study. Twenty isolates representing all seven Sparassis lineages in Wang et al (2004) and eight polypores producing either a brown rot or a white rot were included.

The atp6 region bounded by primers ATP6-3 and ATP6-4 was amplified from 14 Sparassis and 14 polypore isolates with four primers, ATP6-1, ATP6-2, ATP6-3 and ATP6-4 (Kretzer and Bruns 1999), in a modified nested PCR reaction, which performed better in amplifying atp6 products than using one pair of primers in regular PCR setting. PCR reaction mixes (Promega Corp., Madison, Wisconsin) contained 2.5 µL 10x PCR buffer, 5µ M dNTP, 10 pM of primers ATP6-3 and ATP6-4 and 2.5 pM of primers ATP6-1 and ATP6-2, and 5 µL DNA in 25 µL. Taq polymerase was added to the PCR reaction mixes after they were heated to 95 C. The touchdown amplification program included 10 cycles of 94 C for 30 s, 43 C for 1 min, reducing by 0.5 C on every cycle, and 72 C for 1 min, followed by 30 cycles of 94 C for 30 s, 38 C for 1 min and 72 C for 1 min. PCR products were purified with Gene-Clean (Bio 101, Carlsbad, California) and sequenced with the ABI Prism BigDye-terminator cycle sequencing kit (Applied Biosystems, Foster City, California) according to the manufacturer’s protocols. Primers used for sequencing were ATP6-3 and ATP6-4. Sequencing reactions were purified with Pellet Paint (Novagen, Madison, Wisconsin) and were run on an Applied Biosystems 377XL automated DNA sequencer. Sequences were edited with Sequencer version 3.1 (GeneCodes Corporation, Ann Arbor, Michigan) and submitted to GenBank (TABLE I).

The ATP6 dataset was rooted with Climacodon septentrionalis (Binder et al 2005). Parsimony analyses were performed with equal weighting of characters and transformations. Heuristic searches were performed with 1000 replicate searches, each with a random taxon addition sequence. MAXTREES was set to auto increase, and TBR branch swapping was employed. A bootstrap analysis was performed with 1000 replicates, each with 10 random taxon addition sequences, saving ten trees per replicate. MAXTREES was set to 1000, and TBR branch swapping was employed. The NUC dataset was rooted with Lentinus tigrinus, Polyporus squamosus and P. tuberaster (Wang et al 2004). Parsimony analyses were performed the same as the ATP6 dataset. A bootstrap analysis was performed with 1000 replicates, each with 10 random taxon addition sequences. MAXTREES was set to 1000, and TBR branch swapping was employed. Alignments are available at TreeBase (accession number SN2453)

	TAXONOMY

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Sparassis latifolia Y.C. Dai & Zheng Wang sp. nov. FIG. 1a–d

View larger version (35K): [in this window] [in a new window]   FIG. 1. Microscopic structures of Sparassis latifolia Y.C. Dai & Zheng Wang (drawn from holotype). a. Basidiospores. b. Basidia and basidioles. c. Trama hyphae. d. Context hyphae. Carpophorum annuum, solitarium, stipitatum, flabellatum, albidum vel cremeum Systema hypharum monomiticum, hyphae fibulatae vel septatae, hyphae contexti 4.5–9.5 µm diam. Sporae hyalinae, IKI–, CB–, 4.5–5.5 x 3.5–4 µm.

Sporae hyalinae, IKI–, CB–, 4.5–5.5x3.5–4 µm.

Type. – China: Jilin Prov., Antu County, Changbaishan Nat. Res., on the ground in conifer forest, 14-VIII-1997 Dai 2441 (HOLOTYPE in IFP).

Etymology. – Sparassis latifolia, Sparassis species with broad leaf flabellae.

Basidiocarps. – Annual, solitary, stipitate, up to 30 cm high, 25 cm diam, composed of numerous loosely arranged flabellae. Flabellae mostly extend from a common central mass, broad, dissected and slightly contorted, white and soft when fresh, becoming cream colored and leathery with age, pale ochraceous and corky when dry, azonate, up to 1 cm broad, 1 mm thick, margin wavy, sometimes tooth-like. Stipe up to 15 cm long, 1.5 cm thick at base, thinning out.

Hyphal structure. – Hyphal system monomitic; generative hyphae with both clamp connections and simple septa (FIG. 1c, d); tissues unchanged in KOH.

Context. – Contextual hyphae hyaline, thin- to slightly thick-walled, frequently branched, interwoven, (4.5–)5.4–10.5(–11.7) µm diam (n = 30/1). Gloeoplerous hyphae present, refractive, thin-walled, flexuous, frequently branched, 8–14(–16) µm diam (n = 30/1).

Flabellae. – Composed of a hymenial layer, a sub-hymenium, and trama layer. Tramal hyphae hyaline, thin-walled, frequently branched, interwoven, (3–)4.5–9.5(–9.7) µm diam (n = 30/1). Gloeoplerous hyphae present, refractive, thin-walled, flexuous, occasionally branched, 7–12.5 (–13) µm diam (n = 30/1). Hymenia dominated by basidia and basidioles; basidia clavate, with four sterigmata and a basal clamp connection (FIG. 1b), 25–29–2.6–8 µm; basidioles similar in shape to basidia, 20–27–5.4–5.2 µm. Subhymenium distinct and thick, made up of delicate, hyaline, thin-walled, tortuous, densely interwoven hyphae.

Spores. – Basidiospores ellipsoid (FIG. 1a), hyaline, thick-walled, smooth, IKI–, CB– (4–)4.5–5.5(–5.9) x (3.2–)3.5–4(–4.1) µm, L = 5.03 µm, W = 3.85 µm, Q = 1.23–1.35 (n = 90/3).

Additional specimens (paratypes) examined. – China. Jilin Prov., Antu County, Changbaishan Nat. Res., on ground in conifer forest, 14-VIII-1997 Dai 2470 & 2472; 26-VII-2005 Wei 2549a, 2472; 26.VII.2005 Wei 2576.

Other specimens examined. – Sparassis brevipes: Germany: Baden-Württemberg, Karlsruhe, Freudenstadt, Alpirsbach, Baierhof, conifer forest, 24-IX-1995 Kytövuori 96-1044; Freiburg, near Hornberg, Langenschiltach, conifer forest, 27.IX.1996 Laber. S. crispa: Germany: Baden-Württemberg, Freiburg, west of Freiburg, Haslach Rod, Biederbach, Heidburg, mixed forest, 29-IX-1996 Kytövuori 96-1281. Sweden, Vätergötland, Hökensåa, Madengsholm, east of the road 48, pine forest, 18-IX-1984 Kytövuori 84640. Finland: Etelä-Häme, Lammi, Evo, Kotinen virgin forest, conifer forest, 7-IX-1982 Niemelä 2769, 19-IX-1985 Niemelä 3290, 12-IX-1997 Dai 2637.

Sparassis crispa was reported from China and Japan (Tai 1979, Imazeki et al 1988) but Wang et al (2004) and Desjardin et al (2004) found that Asian collections referred to S. crispa are different from European S. crispa both in morphology and molecular characters (TABLE II). Here we describe S. latifolia based on a collection from northern China. This species represents the Asian S. cf. crispa clade in Wang et al (2004). S. latifolia is characterized morphologically by its large, broad, dissected and slightly contorted flabellae and by the production of clamp connections. The species is distributed broadly in east Asia and grows in association with conifers and Fagales. S. crispa and S. radicata also produce clamp connections but they mainly are found associated with conifers. S. crispa might be strictly distributed in Europe and eastern North America while, S. radicata has been found only in western North America. S. cystidiosa also produces clamp connections and, in addition, cystidia. S. crispa was reported from the Russian Far East (Lyubarskii and Vasilyeva 1975), but it probably represents S. latifolia.

View this table: [in this window] [in a new window]   TABLE II. Comparison of Sparassis crispa, S. latifolia, S. radicata and S. spathulata (Data are based on Burdsall and Miller 1988a, b; Martin and Gilbertson 1976; Wang et al 2004; and personal observations)

	PHYLOGENETIC ANALYSES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS TAXONOMY PHYLOGENETIC ANALYSES DISCUSSION LITERATURE CITED

View larger version (18K): [in this window] [in a new window]   FIG. 2. Phylogenetic relationships of Sparassis. a. Parsimony analysis based on atp6 sequences. One of 5780 equally parsimonious trees (length = 1166, CI = 0.486, RI = 0.585). Bootstrap values greater than 50% are indicated along nodes. b. Parsimony analysis based on the combined lsu-rDNA, rpb2 and ITS sequences. One of 16 equally parsimonious trees (length = 1864, CI = 0.627, RI = 0.719). Nodes that collapse in the strict consensus tree are marked with an asterisk above the branch. Bootstrap values greater than 50% are indicated along nodes.

Molecular inference from the NUC dataset.— – The NUC dataset (LSU+ITS+rpb2) had an aligned length of 2326 base pairs (246 ambiguous positions were excluded from the analyses) with 276 uninformative variable positions and 518 parsimony informative positions.

Sparassis species formed a monophyletic group (BP = 90%) with the brown rot fungus Oligoporus rennyi as the sister group (BP = 79%). Sparassis cystidiosa from Thailand was the sister group of all other lineages of Sparassis. Three clampless species, S. spathulata from eastern North America, S. brevipes from Germany and S. miniensis nom. prov. from Spain, formed a clade (BP = 100%), within which three collections of S. spathulata formed a lineage (BP = 100%), and S. brevipes and S. miniensis nom. prov. formed a clade (BP=100%). Three clamp connection producing species, S. latifolia from China, S. crispa from Europe and eastern North America and S. radicata from western North America, formed a clade (BP = 100%), within which there were three groups, including S. latifolia (BP = 98%), European S. crispa (BP = 67%) and S. radicata (BP = 51%). Sparassis crispa from eastern North America was placed as the sister group of S. crispa from Europe without bootstrap support. Within S. latifolia two collections from northern China formed a clade (BP = 76%) while three collections from middle and southern parts of China formed the sister clade (BP = 70 %) to the northern collections.

The major difference between the ATP6 and NUC estimations is that there is no resolution in the S. latifolia-S. crispa-S. radicata clade in the atp6 tree, whereas the NUC tree divides these taxa into two highly divergent clades, one of which contains only S. latifolia. Another noticeable difference between the phylogenies is that S. cystidiosa is the sister taxon of the S. brevipes-S. "miniensis"-S. spathulata clade in the ATP6 analysis, whereas S. cystidiosa is the sister taxon of all Sparassis lineages in the NUC analysis (FIG. 2).

	DISCUSSION

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Phylogenetic relationships within Sparassis species suggested in Wang et al (2004) with lsu-rDNA and ITS data were basically supported by NUC dataset in this study. Among the clamp connection producing species, monophyly of western North American S. radicata was upheld (but with weak bootstrap support of 51%), and Asian S. latifolia and European S. crispa received respectively high (98%) and moderate (67%) bootstrap support. Although relationships among these closely related species were not supported by bootstrap values the S. radicata and S. latifolia clade (FIG. 8 in Wang et al 2004) and the S. radicata and S. crispa clade are consistently resolved (FIG. 2b). Sparassis cystidiosa was suggested to represent the earliest diverging Sparassis species based on an rDNA phylogeny (Desjardin et al 2004), and this is supported here with combined data from three nuclear genes (FIG. 2b). There is virtually no sequence divergence in the atp6 gene among clamp producing Sparassis species. The nuclear gene phylogeny in this study strongly supported S. latifolia as a separate species from S. radicata and S. crispa, but the atp6 phylogeny did not resolve the three species as expected. Nevertheless the atp6 phylogeny agreed with the nuclear gene phylogeny with regard to the relationships among clampless Sparassis species from different geographical regions and supported the divergence of the North American S. spathulata from European S. brevipes and S. miniensis nom. prov.

Because significant divergence of nuclear genes has been observed among S. latifolia, S. crispa and S. radicata, the highly conserved atp6 genes in these fungi could be evidence of clonal inheritance within partly overlapping populations. A decreased mating rate among the three related groups would enhance genetic drift of genes dominant in the population and diminish polymorphism, and a dominant copy of mitochondrial genes would be maintained. On the other hand quick changes in mitochondrial genes would be observed within small and separated populations, which have a less strict sexual incompatibility. Mating behavior may not affect the nuclear genes to this extent, because genetic changes from both partners can be fixed through sexual recombination. Multiple factors are involved in mating compatibility of S. radicata, and successful mating was shown to be more likely between distant isolates (Martin and Gilbertson 1976). However we cannot exclude the possibility that substitution rates of the atp6 gene are extremely low among clamp connections producing species in Sparassis. Data from other mitochondrial genes in Sparassis species are not available for comparison, and the uniformity of the atp6 gene among some Sparassis species is not necessarily evidence of homogenization of mitochondrial genomes of those fungi. Another explanation for the uniformity of the atp6 gene among clamp producing Sparassis species is that these fungi have been isolated geographically through recent radiation events and hybridization among them still exists but at a very low frequency.

Robinson et al (2001) studied the atp6 phylogeny of Agaricus species, and their results were similar to ours. Close relationships among A. bisporus, A. subfloccosus and A. superonatus were supported by rDNA data, and these taxa exhibited little distance in the atp6 phylogeny while several other Agaricus species had comparatively long internal and terminal branches (Robinson et al 2001). Unfortunately there is no rDNA phylogeny of all Agaricus species sampled by Robinson et al (2001), and neither is there information about the mating types of these fungi.

Phylogenetic analyses have been used widely in study of population to phylogenetic classification of higher-level taxa of fungi. Theoretically different substitution rates are expected in genes between populations of different mating behaviors and traits of mating behavior should be traceable in population level phylogenies. Our study demonstrates incongruence between nuclear gene phylogeny and mitochondrial atp6 gene phylogeny within three closely related Sparassis species, which is associated with the presence or absence of clamp connections. We are currently studying the mating behavior, distribution and colonization strategies of these fungi.

	ACKNOWLEDGMENTS

 
We are grateful for Prof. Teuvo Ahti’s (University of Helsinki, Finland) help with the preparation of the Latin descriptions and for two reviewers’ and Dennis E. Desjardin’s helpful comments. David Hewitt (Farlow Herbarium, Harvard University) generously provided some references. The study was supported by the National Natural Science Foundation of China (Grant No. 30425042) to YCD. This study also was supported by grants from the National Science Foundation of the USA (DEB-0228657) to DSH and (DEB-0128925) to DSH and MB.

	FOOTNOTES

 
Accepted for publication April 11, 2006.

Current address for Zheng Wang: Roy J. Carver Center for Comparative Genomics, Department of Biological Sciences, University of Iowa, Iowa City, IA 52242-1324. E-mail: zheng-wang{at}uiowa.edu

¹ Corresponding authors contributed equally to this study. E-mail for Yu-cheng Dai: yuchengd{at}yahoo.com

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