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Phylogenetic Relationships of Cantharelloid and Clavarioid Homobasidiomycetes Based on Mitochondrial and Nuclear Rdna Sequences

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Phylogenetic Relationships of Cantharelloid and Clavarioid Homobasidiomycetes Based on Mitochondrial and Nuclear Rdna Sequences http://www.jstor.org/stable/3761626 . Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. 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 This content downloaded from 130.132.173.57 on Tue, 10 Jun 2014 12:51:21 PM All use subject to JSTOR Terms and Conditions Mycologia, 91(6), 1999, pp. 944-963. ? 1999 by The Mycological Society of America, Lawrence, KS 66044-8897 Phylogenetic relationships of cantharelloid and clavarioid Homobasidiomycetes based on mitochondrial and nuclear rDNA sequences Elizabeth M. Pine1 tion, fungi, Gomphaceae, phylogeny, ribosomal Department of Plant and Microbial Biology, DNA, systematics University of California, Berkeley,California 94720 David S. Hibbett INTRODUCTION Michael J. Donoghue Harvard UniversityHerbaria, Fruiting bodies of cantharelloid and clavarioid and Department of Organismic Evolutionary Biology, Homobasidiomycetes include funnel-shaped or pile- Harvard Cambridge,Massachusetts 02138 University, ate sporocarps with smooth, wrinkled, or lamellate hymenophores, and unbranched club or branched coralloid sporocarps with smooth or folded hymeno- Abstract: data from mitochondrial and Sequence phores. Ecological habits range from saprophytism nuclear small subunit rDNA were used to estimate and parasitism to ectomycorrhizal and lichenized mu- of cantharelloid and cla- phylogenetic relationships tualisms. Anatomical and biochemical diversity is varioid diverse Homobasidiomycetes. Sixty-five found in characters such as spore ornamentation and were in- Homobasidiomycete species investigated, reactivity, hyphal structure, patterns of meiotic divi- 23 cantharelloid and clavarioid Al- cluding species. sion, secondary compounds, and chemical structure nodes in the tree could not be though deep resolved, of pigments (TABLE I). four cantharelloid and clavarioid lineages containing Although all modern authors agree that the can- were identified. Cantharellaceae fungi (i) (Canthar- tharelloid and clavarioid fungi are polyphyletic (e.g., ellus, Craterellus) is closely related to Hydnum, which 2, 4, 10, 11, 12, 14, 19, 21, 24, 43, 58, 72, 74, 83), is which is a and toothed, Stichoclavaria, simple club, evolutionary relationships of monophyletic taxa have which is coralloid. These taxa all have Clavulina, not been resolved. Relatively few morphological char- stichic nuclear which is a division, synapomorphy acters have been identified that can be compared this clade. is supporting (ii) Clavariadelphus closely across genera, and many of these support incongru- related to and Ramaria. This is Gomphus relationship ent relationships. Various authors have emphasized reactions of treated supported by green sporocarps different suites of characters and consequently have with iron which is reflective of the of salts, presence proposed conflicting evolutionary histories (e.g., 10, the The nearest relatives of compound pistillarin. 12, 14 vs 19 vs 72). A preliminary phylogenetic anal- these cantharelloid and clavarioid are fungi gastero- ysis using published morphological characters failed the earth star the stink- mycetes, including Geastrum, to resolve relationships among genera of cantharel- horn and the "cannon-ball Pseudocolus, fungus" loid and clavarioid fungi (EM Pine unpubl). Results The clavarioid Cla- Sphaerobolus. (iii) fungi Clavaria, presented here use DNA sequence data as an inde- and to be derived vulinopsis, Pterula, Typhula appear pendent and abundant source of characters for com- from the that contains most of the fun- lineage gilled parisons across diverse lineages. Clavicorona is related to gi. (iv) closely Auriscalpium, This discussion treats only taxa and characters rel- which is and which is toothed, Lentinellus, gilled. evant to results of this study. Corner (10, 12, 14), This is united ornamenta- lineage by amyloid spore Donk (19), and Petersen (74) provide broad taxo- tion. these results that there has Although suggest nomic reviews of cantharelloid and clavarioid fungi. been extensive in mor- convergence fruiting body Selected authors' taxonomic treatments of key gen- phology, certain anatomical and biochemical features era are summarized (see TABLE II). to be appear phylogenetically informative, notably Cantharelloid and clavarioid fungi figure promi- stichic nuclear of and division, presence pistillarin, nently in hypotheses about the origin of the fleshy or of ornamentation. cyanophily amyloidity spore basidiomycetes (12, 15, 31, 32, 43, 58, 72, 83, 84). Words: evolu- Key Cantharellaceae, Clavariaceae, Their fruiting forms can be arranged in a transfor- mation series, with simple clubs at one extreme, can- Accepted for publication June 10, 1999. tharelloid forms intermediate, and agaric forms at 1 Email: [email protected] the other extreme. Corner (15) proposed the "Cla- 944 This content downloaded from 130.132.173.57 on Tue, 10 Jun 2014 12:51:21 PM All use subject to JSTOR Terms and Conditions PINE ET AL: CANTHARELLOID AND CLAVARIOID PHYLOGENY 945 varia theory" of basidiomycete evolution, which Gomphaceae to the Paxillaceae" (83 p 126). Peter- treats the cantharelloid and clavarioid fungi as a basal sen (69) concluded that Linderomyceswas a synonym paraphyletic group from which all other Homobasi- for Gloeocantharellus, a gomphaceous genus whose diomycetes have been derived. Corner suggested that morphology has been described as intermediate be- the simple club with a smooth hymenophore (e.g., tween Cantharellus and Gomphus (81). Corner (12, Clavaria) is the ancestral state of the fleshy fungi, 15) and Petersen (71, 72) agreed with Singer that from which have been derived first club-shaped and Gloeocantharellus/Linderomycesbelongs in Gompha- cantharelloid intermediates with folded hymeno- ceae, but thought it could represent an evolutionary phores (e.g., Clavariadelphus and Cantharellus, link with Paxillaceae and some Boletaceae. whose hymenial configurations differ from true la- Anatomical features suggest that cantharelloid and mellae in the orientation of hyphae in the trama), clavarioid fungi comprise several independent line- and eventually gilled mushrooms. Corner's model ages (TABLEI). Spore morphology can be used to has had a strong influence on subsequent evolution- delineate three groups. Hyaline, unornamented ary hypotheses. For example, Julich (43) suggested spores that do not react to Meltzer's reagent or Cot- that Clavariaceae was derived from the Auriculariales ton Blue are characteristic of most of the known can- (jelly fungi) or their ancestors, and that Cantharel- tharelloid and clavarioid fungi. Spores with distinc- lales is the basal group of Homobasidiomycetes. Mill- tive amyloid ornamentation are found in the coral- er and Watling (58 p 439) state that "the logical ex- loid genus Clavicorona;Donk (19) used this feature, tension from the clavarioid condition among epige- along with presence of gloeocystidia, to transfer Cla- ous taxa is the cantharelloid basidiome," and suggest vicorona from Clavariaceae to Hericiaceae. The re- that agarics have been derived multiple times from maining spore type, ochraceous with cyanophilic or- cantharelloid ancestors. Other authors agree that namentation, is found in genera with a variety of there must have been transformations among coral- fruiting body forms: Gomphus (cantharelloid), Ra- loid, cantharelloid, and agaric forms, but propose the maria (coralloid), Beenakia (hydnoid), Kavinia and opposite polarity, suggesting that lineages containing Ramaricium (resupinate), and Gloeocantharellus (= cantharelloid, coral, and club fungi have been de- Linderomyces) (agaric). Despite their macromorpho- rived from agaric ancestors (2, 30, 72, 83). logical diversity, these taxa have been grouped in The agarics Hygrocybeand Gerronema have been Gomphaceae (18, 19, 21, 44, 46, 52, 71, 83), a place- suggested as close relatives of Cantharellaceae. Hy- ment that is supported by shared green reactivity of grocybeis similar to Cantharellusin having thick, waxy, fruiting bodies treated with FeSO4. The club-shaped decurrent gills, bright orange and yellow pigments, genus Clavariadelphusalso reacts with ferric salts, but long and narrow basidia, and hyaline, unornament- has smooth, hyaline, unornamented spores (56). If ed, non-reactive spores (34). Gerronema(= Omphal- macrochemical reactions and mode of nuclear divi- ina) chrysophyllum resembles members of Cantha- sion are emphasized, Clavariadelphus is placed with rellaceae in spore color, hymenial anatomy, basidio- Gomphaceae (2, 19, 30, 32, 56, 72, 90), but emphasis carp color, general aspect, and molecular structure on spore morphology supports a relationship with of carotenoid pigments (2, 29, 48, 83). Yet chante- Cantharellaceae or Clavaria (10 p 25, 11, 12, 14, 58, relles depart from true mushrooms in several impor- 65, 68, 72). tant characters (TABLE I), including anatomical dif- The position and orientation of the first nuclear ferences between cantharelloid gill-folds and true division of meiosis has been proposed as a taxonom- agaric gills
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