Perspectives in the New Russulales
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Mycologia, 98(6), 2006, pp. 960–970. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 Perspectives in the new Russulales Steven L. Miller1 INTRODUCTION Botany Department, University of Wyoming Friesian concepts stressing macromorphological ap- Ellen Larsson pearance of sporophores dominated classification Karl-Henrik Larsson systems in the homobasidiomycetes until the mid- to Plant and Environmental Sciences, Go¨teborg late 20th century. Before that time resupinate, agaric, University, Sweden coralloid and gasteromycete fungi were considered Annemieke Verbeken more closely related within each sporophore type and Jorinde Nuytinck it was inconceivable that taxa with diverse sporophore morphologies could be classified together. Biology Department, Ghent University, Belgium Donk (1971) recognized the possibility that the Hericiaceae was related to other basidiomycetes with Abstract: The Russulales is one of 12 major lineages a variety of sporophore types because these fungi all recently elucidated by molecular sequence data in the possess a system of gloeoplerous hyphae and amyloid ornamented spores. ‘‘All these taxa may eventually be homobasidiomycetes. The order is morphologically considered as part-chains of one big system without most diverse, containing a remarkable variety of necessarily losing their status as distinct families,’’ sporophore forms including resupinate, discoid, ef- Donk said. ‘‘They might appear to be members of one fused-reflexed, clavarioid, pileate, or gasteroid and big order, but then certainly an order also containing hymenophore configurations from smooth, poroid, quite a number of reduced species or genera in which hydnoid, lamellate, to labyrinthoid. Functionally these the original, most prominent features chosen for its fungi are primarily saprotrophs but others are ectomy- characterization have vanished.’’ At about the same corrhizal, root parasites and insect symbionts. A time Singer and Smith (1960) questioned the phylogenetic analysis of the nuclear 5.8S, ITS2 and necessity of maintaining a separation between agarics large-subunit rDNA genes comprises the best informa- and sequestrate or gasteroid taxa in the Hymenogas- tion to date on relationships of taxa within the trales. Oberwinkler (1977) proposed the Russulales as Russulales. Two large sister groups encompassing 11– an example of a closely knit group of fungi that 13 major clades have been recovered within the included all possible types of sporocarps known Russulales. Based on molecular and morphological data among homobasidiomycetes. This concept has gained 12 families and approximately 80 genera have been acceptance and underpins the classification used the identified, although placement of many taxa has not yet Dictionary of Fungi (Kirk et al 2001). been determined. The two clades containing ectomy- Monophyly for the Russulales has been confirmed corrhizal taxa, corresponding to the Russulaceae and through DNA sequence analysis numerous times over the Albatrellaceae, represent the greatest diversity of thepastdecade(HibbettandDonoghue1995, sporophore morphologies. The primarily pileate lamel- Hibbett et al 1997, Bruns et al 1998, Hibbett and late family Russulaceae is nested with resupinate species Binder 2002, Larsson and Larsson 2003, Larsson et al and also contains pileate sequestrate, gasteroid annulate 2004, Binder et al 2005). Miller et al (2001) explored and pleurotoid forms. Albatrellaceae similarly contains the molecular phylogeny of the agaricoid, gasteroid resupinate poroid, pileate poroid and pileate labyr- and pleurotoid taxa in the Russulales, now more inthoid sporophores. Presence of gloeoplerous hyphae appropriately called the Russulaceae. Larsson and containing fluid that typically stains black in sulfoalde- Larsson (2003) provided a detailed study of russuloid hyde compounds is a synapomorphy for the Russulales. aphyllophoralean taxa but included also representa- Amyloid reactions in spore or hyphal walls that occur tives with most of the different sporophore morphol- frequently throughout the Russulales often are per- ogies. The goal of this paper is to present the most ceived as an obvious synapomorphy but are inconsistent. complete molecular data for the Russulales. Approaches including sequencing functional genes, analysis of gene expression and biochemical analysis across the entire order are needed. MATERIALS AND METHODS Key words: fungi, homobasidiomycetes, russuloid Sampling of taxa for this analysis was guided by Miller et al (2001) and Larsson and Larsson (2003), recent sequencing Accepted for publication 20 September 2006. efforts, and by sequence availability in GenBank. Taxon 1 Corresponding author. E-mail: [email protected] sampling included only OTUs with complete nLSU, 5.8s 960 MILLER ET AL:RUSSULALES 961 and ITS2 sequences. Sequence data from other gene form a typical palisade hymenium, while others form regions were available for some taxa, however including a catahymenium (Lemke 1964) where the basidia these data would have resulted in an unacceptably large originate deeply within the thick-walled hyphidia and amount of missing data. Taxa sampled, GenBank accession just reach the surface. These sporophores are adapted numbers and morphological and cytological features, are to resist drought and can quickly resume sporulation provided (SUPPLEMENTARY TABLE I). in favorable conditions. In the present study no clear Molecular techniques and methods of phylogenetic topological break supported the /amylosteriaceae or analyses were essentially identical to those found in Miller et al (2001) and Larsson and Larsson (2003), and for the /gloeocystidiellum II as separate from the Peniophor- sake of brevity in this volume we direct the reader to those aceae. The remaining well supported clades corre- citations. The alignment for this study has been submitted sponded to the /eurussuloid clade of Larsson and to TreeBASE as No. SN3256. For discussion provisional Larsson (2003). names have been assigned to individual families, although Amylostereaceae (bootstrap support 100%).—The pres- these might not constitute formally valid names. ent analysis found strong support for the Amyloster- eaceae composed of three leathery effused-reflexed RESULTS AND DISCUSSION species with a smooth hymenophore. This differs dramatically from Larsson and Larsson (2003) who Molecular analysis.—At present, based on molecular recovered a group composed of Amylostereum and and morphological data, the Russulales comprises 12 Artomyces, which has a clavarioid sporophore. Arto- families and approximately 80 genera (SUPPLEMENTA- myces in the present analysis was associated consis- RY TABLE II) and 4000 species worldwide. More than tently with the Auriscalpiaceae, and this relationship one-third of the species belong in two mainly pileate has been observed in other molecular studies as well lamellate genera in the Russulaceae: Russula and (Hibbett et al 1997, Hibbett et al 2000, Hibbett and Lactarius. Included in the 80 genera are many still Donoghue 2001). poorly known fungi for which no sequence data are available and their placement in families has been Auriscalpiaceae (bootstrap support 65–90%).—The difficult. Families include Albatrellaceae, Amylostere- Auriscalpiaceae was erected by Maas Geesteranus aceae, Auriscalpiaceae, Bondarzewiaceae, Echinodon- (1963) to contain resupinate hydnoid (Dentipratulum tiaceae, Gloeocystidiellaceae, Hericiaceae, Hybogas- and Gloiodon) and pileate hydnoid (Auriscalpium, teraceae, Peniophoraceae, Russulaceae, Stereaceae FIG. 1A) taxa as well as pileate lamellate (both and families containing Aleurocystidiellum and Gloeo- agaricoid and pleurotoid) taxa (Lentinellus,SUPPLE- dontia that have not been described formally. Eleven MENTARY FIGURE 1C). Most of the species with hydnoid to thirteen major well supported clades have been hymenophores are moderately tough with dimitic elucidated within the Russulales with 11 identified hyphal systems and are sister to a clade containing the (FIG. 2). In a neighbor joining analysis Larsson and soft or slightly leathery Lentinellus spp., and it could Larsson (2003) recovered a topology for the Russu- be argued that these represent two closely related but lales placing these major clades into two larger distinct families. groups, the /peniophorales and the /eurussuloid The genus Artomyces (FIG. 1B) is composed of clades, which could be considered suborders. lignicolous, branched clavarioid taxa found through- out temperate regions of the northern hemisphere FAMILIES AND FAMILY CHARACTERISTICS (Ju¨lich 1981). A clade with several Artomyces species typically forms a sister clade with Lentinellus.If Peniophoraceae (bootstrap support 100%).—In the Artomyces is excluded from the clade support for present analysis the Peniophoraceae, roughly equiva- the Auriscalpiaceae is 90%; if Artomyces is included lent to the /peniophorales recovered by Larsson and bootstrap support falls to 65%. Larsson (2003), comprises primarily saprotrophic Gloeodontia family (bootstrap support 100%).—The fungi with resupinate, discoid or clavarioid sporo- Gloeodontia family includes primarily resupinate fungi phores with smooth hymenophores (FIG. 1D, E) and with tough dimitic hyphal systems and hydnoid weakly or nonamyloid spore walls. The insect symbi- hymenophores as well as at least one species with ont Entomocorticium also has been tentatively placed a monomitic hyphal system and smooth hymeno- here (Hsiau and Harrington 2003). The fresh phore. Dimitic taxa in the group have