Mycologia, 82(1), 1990, pp. 48-58. O 1990, by The New York Botanical Garden, Bronx, NY 10458-5126

HETEROGASTRIDIALES: A NEW ORDER OF BASIDIOMYCETESl

FRANZ OBERWINKIER, RoBERT BAUER

Lehßtuhl Spezielle Botanik und Botanischel Garte , Universität T biigek, Auf der Morgenslelle l, D 7400 Tübingen 1, lryes Germany

AND

RoBERT J. BANDoNI

Department oJ'Bolany, Univetsitv of British Columbia, Vancouver, B.C. Y6T 281, Canada

ABSTBACT

Descriptions are provided ofnew basidiomycetous taxa based upon the leleomorph of Hyalopycnß blepharistama, the laxa arc: . Heterogaslridiaceae, Heterogaslridium, a\d Hetero- gastidiu»l pycnidioideurr. Thetype species is characterized by a pycnidioid basidiocarp with an intemal basal hymenium. Phragmobasidia produce sessile, digitately branched basidiospores that are released passively. Ontogeny oflhe basidia, basidlospores, and septal pores has been studied. The septal pores are simple. bu1 vary morphologically during ontogeny. Hyphal cells. conidiogenous cells, and conidia are dikaryotic. The structure oflhe spindle pole body indicates helerobasidiomycetous affinities. Key Words: Heterogasiridiales, Heterogasl diaceae, Eeterogastridium pycnidioideum, Hyalopycnis b lep har is t o ma, Heterobasidiomycetes, gastroid basidia. pycn jdia

Hyalopycnis blephdristoma (Berk.) Seeler is stuhl Spezielle Botanik, University of Tübingen; widely dislributed and has been reported fiom some also have been deposited in the IFO, Osaka, Austria, England. Japan, and North America (von and ATCC culture collections. Cultures were Höhnel, l9l8; Petch. 1943: Seeler, 1943i Tubaki, maintained on mah yeast peplone (MYP, Ban- 1969; Bandoni and Oberwinkler, 1981). Bandoni doni, 1972) and were grown oD this medium, oat and Oberwinkler (1981) studied morphology and flake agar (OFA). potato-dextrose agar (PDA) development of the species and found suflicient with l0 g sucrose per liter of medium, and Difco characters to rdentify H. blephaistoma as a ba- Corn Meal Agar (CMA) fortified with 0.5 g Difco sidiomycetous anamorph. Although tetraradiate yeast exlract per liter of medium. Cultures were cells were also observed sporadicallt, du ng that incubated at 20 C in incubators with i2 h lighL/ study, they were not artached to basidia when l2 h dark cycles and fluorescenr lighling. seen and were mistakenly thought to be another We also subjected cultures to the common pro- conidial form. Basidia were iater found in sub- cedures used in slimulating sporulation in aquat- stanlial numbers in the pycnidioid sporocarps of ic hyphomycetes in atlempls to induce basidial one ofthe several strains sludied. developmenl. The procedures included daily flooding and draining of one week old cultures on MYP or on OFA (Bandoni and Tubaki, 1985), covering such plate cultures with a layer ofsterile The strains of H. blepharisto ta used in this waler, submersion of blocks of agar and myce- study are listed in TnaE I; all are deposited in lium in sterile, still water (Ingold, 1942), and the culture collections ofthe Department ofBot- submersion in aemtedwater (Marvan et a|.,1979). any, University of B tish Columbia and Lehr- AII cytological and morphological illustrations shown here were obtained using a single strain ' Pan 57 of a series. "Studies in Heterobasidiomy- (CTR cetes" ofthe Institure of Biology I, University ofTü- of H. blepha stoma 66-90). Living and bingen, and the Department of Botany, University of fixed material was examined with a Zeiss pho- British Columbia. tomicroscope III, using phase optics and No-

48 OBERWTNxTER Er la. : HETERocAsTRIDIALES 49

TABLE I IsoLA'fEs oF HyaropycNls BLEpH)RIsroMA usED tN THts sruDy

Culture Other nos. Source and location

cTR 66-90 ATCC 48561 On old agaric, coll. New York, S. J. Smith No. 40782 cTR 69-137-t ATCC 48563 On Scleroderma aurantium patasitized by Sepedomium chrysosper ,irm, New York, C. T. Rogerson cTR 70-135 ATCC 48560 On H maria hemispherrca, New York, C. T. Rogeßon cTR 78-131 ATCC 48562 On Amanita sp. patas\tized, by Hypomyces hyalirLs, New Yo*, C. T. Rogerson TY 4211-C-5 rFo 8906 From rotlen pumpkin harvested in Sapporo, T. Yokoyama zuB 6063 UBC 75-6063 From litter of Orerc,,s yirg,rirara, New Odeans, LouisiarE, R. J. Ban- (1-3) doni RJB 6649 UBC 75-6649 From decaying tomato plant, Vancouver, BC, R. Bandoni

marski interlerence contrast optics. For trans- OBSERYATIONS mission electron microscopy, samples were flxed in 20lo glutaraldehyde in 0.1 M sodium cacodylate None ofthe experiments involving wetting or buffer at pH 7.2 for periods ranging from over- submerging mycelium of H. blepharistomq were night to several days. Following six transfeß in successful. Plates in such tests were scanned for 0.1 M sodium cacodylate buffer, material was the presence of tetraradiate basidiospores and postfixed in l0lo OsO, in the same buffer for two numerous pycnidia were examined for the pres- hours in the dark. washed in distilled water, and ence of basidia. However, no increases in fre- stained in 10/o uranyl acetate solution for I hour quency of basidiospores or basidia could be de- in the dark. After five washes in distilled water, tecled alter any lrealment. Nor were increases in the material was dehydrated in acetone, using 10 basidiospore production observed when strains minute changes at 25o/o, 5oo/o,'70o/o, 950/o, ar,d.3 were grown on different media. Basidia were x 1000/0 acetone. The material was then embed- found only in CTR 66-90, and this occurred ded in Spurr's plastic (Spurr, 1969). Series of without water treatments or changes in media. sections were cut on a Reichert ultramicrotome The following observations on teleomorph mor- using a diamond knife. The sectionswere mount- phology and development thus are based only ed on Formvar-coated single-slot copper grids, upon that stmin. stained with lead citrate (Reynolds, 1963) at room Basidiomes arise from a loose hyphal network temperature for 3-5 minutes, then washed again (FIG. 1) of mostly simple-septate, thin-walled, with distilled water. Seclions were examined with smoolh hyphae. 2-3 /m in diam. Sporocarp pri- a Zeiss EM 109 lransmission electron micro- mordia differentiate into a cluster ofgenerative scope at 80 kv. hyphae around which the sterile peridial hyphae

Frcs. l-5. Line drawings of Hetercgastridium pycnidioideum. 1. RecoDstructed sectional sketch ofa basidi- ome showing intemal hymenium with basidia in different developmental stages, basidiosporcs, co diophores, and conidia 2-5. stages in basidial ontogeny. 2. several young probasidia, showing nucleiand nucleoli,;epate basidium with basidiospore initials, and one in which the basidiospores are almost mature. 3. upper portion ol a basidium showing slight asynchrony in basidiospore development and vacuolization ol spoie-producing cells. 4. Detail of basidial apex and developing basidiospore. 5. Podion ofbasidium with mature basiäiosporesi

FIos. 6-12. Basidiocarys and different stages in development ofbasidia, basidiospores and conidia of ller- pycnidioideum. yo,rng erogasrridium 6. pycnidioid basidiome seared on a basal network of hyphae (bar = 50 Pm) Note apical divergence ofneck cells. 7. Lower portion ofbasidiome showing intemal basai irymenium (bar : 30 pm). 8. Slightly squashed hymenium showing basidia and basidiospore; (bar : 30 pm). 9. Clustei of conidiophores, some conidiogenous cetls ofwhich bear conidia (bar = 20 &m). 10. Hymenium with one old young basidium, several basidia, and neighboring conidiogenous cells and conidia lbar = 2b pm). I l, 12. Delached basidiospores, two ofwhich have anastomosed after germinating (bars = 20 pm). I l. conidium formation after fusion oftwo basidiospores. 6-7. Brighl-freld microscopy. 8. Nomarski interference contrast micrcscopy. 9-12. Phase contrast microscopy. 50 MYCoLocrA

T 10pm

1 OsrRwrNKrpn rr,lr.: HETERoGASTRIDIALES

-,7':)

( /\

10

l1 12 52 MYCoLocrA

\\ a\ l3 t4 ,\

t a o

ta

l8 ',;': ä OBERWINKLER TT,{a.: HETERoGASTRTDTATES 53

develop. A single layer of the peridial hyphae, 25 rrm in outline, and the arms are 2-3(4) pm each cell 8-15(-20) pm diam and 100-500(-800) diam. The basidiospores are released passively irm long, form both the swollen base and the and accumulate in large quantities, generally ad- tapering neck of the basidiome. The neck is of mixed with conidia (Frc. l), in a slime drop at vadable length and 40-100 pm diam, the cells the apex of the basidiome. FrcuRES 6-8 show lapering gradually apically and diverging sharply youlg developmental stages, the basidiomes not near lheir apices (FrcS. l, 6). The peridial cells yet filled with spores. For the sake ofclarity, only are only weakly adherent to one another and a few spores have been illustrated in Frc. l. Ba- often separate in microscope preparations. The sidiospores germinate by germ tube and these generative hyphae form a densely interwoven often fuse with other spores or germ tubes (FIcs. basal subhymenium (Frcs. I, 7, 8) which mostty I 1, l2). Often short hyphal outgrowths terminate bears a mixture of conidiophores and basidia by conidium production (Frc. I l). (Frcs. 1, 10). with age, the hymenium thickens The basidiomes examined always had conid- considerably by proliferative growth of genera- iophores intermixed with basidia in the hymeni- tive hyphae (Frc. l). Basidia develop succes- um (Frcs. 1, 10). The presence ofbasidiospores sively (Frcs. 2, 10, 16). and conidia is also proof of the simultaneous Youngbasidia have diploid nuclei (Frcs. 2, 13) production of sexual and asexual propagules in and are cylinddcal or sometimes tapering, the the same sporocarps. The conidiogenous cells are cytoplasm densely and conspicuously granular. unusual in that each produces a single conidium, The diploid nucleus, 4-5 x 5-6 pm, and the i.e., they are monoblastic (Frc. 9). Duringconidi- nucleolus which is ca I pm diam are easily visible al development, as during that of basidiospores, with phase contrast and Nomarcki interference cytoplasm empties from the sporogenous cell into contrast optics (Frcs. 13, 14, 16). Post-meiotic the growing conidium. This type ofconidial de- basidia are transversely 3-septate, 5-8 x 60-80 velopment also occurs in the basidiomycetous pm (Fros. l-3, 10, l4-18), and each cell develops atamorph Nai adel la fluitans Marvanovä & Bat one basidiospore. The site ofspore outgrowth is doni (Marvanovä and Bandoni, 1987). apical on the terminal cell and distal, i.a, near Septa of H. blepharisloma hyphae have simple the upper septum and laleral. in the remaining pores, the ontogeny of which has been studied cells. Basidiospore development on a single in detail (FrGs. 21-30). Before reaching a mini- meiosporangium is predominantly synchronous mum width of 0.06-0.08 pm, the septal pore (FIcs. l, 2, 4, 5, 10, 14-18), but differences oc- consists of an unstructured opening in the cen- casionally occur (Frc. 3). tripetally growing septum (Frc. 2l). In further Basidiospore initials are at first tubular (Frcs. development, electron-dense bodies occur on 2, 3, 14, 15\ and, after reaching 8-12 pm long, bolh sides ofthe pore (Frcs. 22-25). Such bodies apical enlargement occurs (Frc. 3); 3 or, infre- are a1flrst inconspicuous and 0.02-0.03 pm thick quently, 4 radiating branches then develop (Frcs. (Frc. 22); finally they are 0.06-0.08 pm thick l,2,4, 5, 10, l6-18). As the spores grow, vac- (Frc. 25). These stages show mostly electron- uoles enlarge in the basidial cells (Frcs. 2, 3, 5, transparent septal walls (Frcs. 2l-25);onty faint, 10, l5-18). Mature basidiospores are separated electron-dense striations of wall material can be from basidial cells by basal septa (Ftcs. 5, l8) at rccognized (Frcs. 23, 24). Older developmental which time the old basidial cells are empty (FrGS. stages show thicker septal walls with multilay- 5, 18). The predominantly tetraradiate basidio- ered electron-dense parts separated by a middle spores (Frcs. ll,12,17,l8)measure8-13 x 15- Iayer of electron-transparent matedal (Frcs. 28-

Frcs. 13-19. Diferenl slages of basidial development aDd spindle pole bodies (spBs\ in Heterogestridillm pycnidioideum. 13. Young aseptate basidia (note nuclei and nucleoli) and associated conidiogenous äl bearing conidium (bar: 2o pm\. 14, 15. Aseptate and young septate basidia, the larter with very y-oung basidiospor! initials (bars = 20 pm). 16-18. Basidia with altached basidiospores. Nole correlation of vaiuötario,-n ano basidiat development (baß : 2O pm} 19,20. Spindle pole bodies (SpBs) showing conspicuous middle pie"" .na i*o marginal discs (bars : 0.2 pm). 19. Mitotic interphase spB. 20. prophaie I sFB. 16. Nomarsii intederence contrasl microscopy. 13-15, 17, 18. Phase contmst microscopy. 19-20. Transmission electron microscopy. 54 MYCoLocrA

;21 J ir: "r. -;

':,t';* #r, §:'i&.-, '1,4I

i;i-t-. ': t'e) t iti.+ )'i. -

-.i

*29 tsü** OBERWIN'KLER -E r ,{a. : HETERoGASTRIDIAIES 55

30). The electron-dense bodies fuse and occlude pm diam. Hyphae muri pycnidii 8-15(-20) pm diam. the septal pore. Final stages ofcell aging may be Basidia longi-cylindracea, 5-8 x 60-80 pm, mature transverse septata. Basidiosporae recognized by large vacuoles and a thin layer of sedentes, tetraradia- tae, raro pentaradiatae. 2-3 !m diam. ambitu 8-13 x cytoplasm attached to the cell walls. The septal l5-25 pm. pores at this time are completely plugged with TYPUS: F. Oberwinkler 36439 (M). electron-dense material (Frcs.29,30) and the pore may be overgrown by additional wall layers DISCUSSION (Frc. 29). Von Höhnel (1918) described two species As viewed in longitudinal section, the inter- of Hyalopycnis, H. hyalina and, H. Nitea, b:utthese phase or prophase spindle pole body (SPB) con- were later considered be identical (Seeler, sists ofa conspicuous electron-dense middle part to 1943). Seeler found that the species was identical and two peripheral discJike portions (Frcs. 19, to Sphaeronema blepharistoma Berk. The de- 20). The discs are surrounded by electron-opaque scriptions by both von Höhnel and Seeler clearly malerial. The middle pan is in close proximity refer to fungi imperfecti, although Seeler illus- to the nuclear envelope. Osmiophilic material is trated two basidiospores and referred to thesc as present close to the inner surface of the nuclear "cruciform bud-spores." Bandoni and Ober- membrane, adjacent to the SPB. winkler (1981) described and illustrated the mor- phological characteristics of Ff. b lep haristo ma as seen by light microscopy and concluded that the The characteristics of the teleomorph of 1lr,- dikarlolic hyphae, infrequent clamps, posilive alopycnis blephaistou 4 are unique, and they were Diazonium Blue B, and chlamydospore devel- not included in the descdptions of von Höhnel opment all indicated a basidiomycetous rela- (1918) and Seeler (1943). A new , lletero- tionship. That assumption is now verified by ba- gastridium Oberwinkler & Bauer, is therefore sidial production in axenic culture. proposed to accommodale this unusual . PycnidiumJike pycnia or spermogonia are present as haploid developmental stages in the Heterogastridium Oberwinkler and Bauer, ger. life histories of many Uredinales, some ofwhich may resemble the "pycnidia" of H. blepharis- roza morphologically. However. rusl pycnia are pycni- Genus Helerobasidiomycelum. Carposoma haploid and are functionally different from pyc- dioideum, hyphis enodulosis parce nodulosi-septatis, distinctis, hyalinisque compositum. Septa hypharum nidia ofthe tatter. Only a few basidiomycetes are simpliciter perforata sunt. Cystidia desunt. Basidia lon- known Io produce dikaryotic pycnidioid sporo- ga, mature transverse septala, sine sterigmatibus inde carps to date: they include Fibulocoela indica basidiosporae non modo sedenles sed etiam non eiec- Nag Raj (Nag Raj, 1978), H. blepharistoma(Bat tae sunt. Basidiosporae hyalinae, tenui-tunicatae, tuni- guaduae cis levibus, hyphas angustas germinando producunt. doni and Oberwinkler, 1981), Ellula Plurimum fructificationibus pycnidioideis anamor- (Viegas) Nag Raj (Nag Raj, 1980), arrd Mycau- phosium in cultura pura. reola dilseaeMaie & Chemin (Porter and Fam- TYPUS GENERIS: HeterogasÜidium pycnidioi- ham, 1986). So far as is known, the only one of /prn Oberwinkler er Bauer. opus rpsum. these taxa in which basidia develop in pycnidioid basidiomes is 1L blep haristorna. Hetercgasüidi- Heterogastridium pycnidioideum Oberwinkler um pycnidioideum and its anarnotpt! H. blepha- and Bauer, sp. zor. ristoma, haye identical sporocarp wall mor- Fructifrcatio minuta, pycnidioidea, hyalina, 150-500 phologies and these differ sharply from the walls pm, raro ad 800 pm longa. Hyphae hyalinae, 2-3(-5) of all other pycnidioid basidiomycetes.

FrGs. 2l-30. Transmission eleclron micrographs showing septal pore onlogeny in Hetetugastridium pycnidi- oideum (bdts:0.2 pra). 21. Early developmertal stage without electron-dense bodies and theieptal wal;iectron transparent. 22. Initial stage in development oflhe pore-associated electron-dense bodies. 23-25. Well developed electron-dense bodies, the septal wall electron-opaque. 26-28. Mature septal developmental stages, showing fusion of the electron-dense bodies and partial occlusion of the pore. Two electron-dense layers, ieparated b! an inner electron-transparent layer, are visible in rhe septal wall. 29, 30. Old septa with completely occludeä pores and with additional wall layers deposited on one side ofthe pore in Frc. 29 and on both sides in Frc. 30. 56 MYCoLoGTA

The stilboid, gastero-auricularioid heteroba- frequent, varying with the strain and stage of sidiomycetes were suNeyed by Oberwinkler and development, i.e., they are most commonly pres- Bandoni (1982a) and an order, Aüactiellales, was ent in germ hyphae emanating ftom chlamydo- proposed to accommodate the group. Species in spores. Hyphae with clamps are nol common in the Atractiellales mostly have synnemata-like gasteroid heterobasidiomycetes, but they do oc- basidiomes and transversely septate basidia; cur in species of Phleogena and Afiactogloea aseptate clavate basidia are characle stic of (Oberwinkler and Bandoni, 1982a, b). Clamps Pachnocybe a;ad C hionosp haeru specles. The ba- are also present in so rne runsl:udied Pachnocybe - sidiospores in this group are generally sessile, tike Asian species of gasteroid heterobasidiomy- although those ofSlilbum tulgare are briefly ped- cetes (u[publ. obs.). icellate. Basidial cells in species of Agaicostil- Heterogastridium pycnidioideum has simple bum ar,d Atractogloea bud off numerous basid- septal pores as characteristic in the majority of iospores; single basidiospores are produced by gasteroid auricularioid heterobasidiomycetes basidial cells in species of Atractiella, Stilbum, (Oberwinkler and Bandoni, 1982a) and, in fact, and Phleogena (Oberwinkler and Bandoni, 1982a, of most auricularioid fungi (Oberwinkler, 1985). b), as in fl. pycnidioideum. These taxa ditrer Species of the genera Auricularia (Sebald, 1971 , markedly from H. pycnidioideum in numerous Moore, 1978t Patton and Marchant, 1978; Tu other features. However, there may be a parallel and I(imbrough, 1978; Mclaughlin, 1980) and in spore dispersal between the two groups. Some Myliltopsis (Oberwiokler, 1985) are the only gasteroid audcularioid taxa, e.g., species of known auricularioid fungi with dolipore septa Atractiella and Stilbum resemble the "stalked and parenthesomes .'ft,e ontoger,y of H. pycnidi- spore drops" discussed by Ingold (Ingold, 1961); oideum septal pores was studied in detail (FIcs. it H. pycnidioideum, propagules also accumulate 21-30). It is dificult to compare these with other in the apical slime drop. It is likely that either auricularioid fungi, since few species have been arthropods or water (or both) are responsible for examined in detail. The periphery of the elec- dispersal of spores in both groups. tron-dense bodies which develop adjacent to the Tetmradiate basidiospores occul in some ba- septal pore (FIGS. 22-25) is not sharply delimited sidiomycetes, e.9., in Digitqtispora marina Do- from the cytoplasm and the bodies thus appear guet and Nia ,lälr'ssa Moore and Meyers. In D. to be distinct from Woronin bodies of Asco- mari a the basidia are not enclosed in pycnidi mycetes. Pore occlusions in mature and old septa oid basidiomes (Doguet, 1962). Basidiospores of (Frcs. 26-30) resemble those illustrated and de- Nia librissa are predominantly 5-radiate (Do- scribed as "pulley wheel plugs" in certain rusls guet, 1967), the threadJike branches originating (reviewed by Littlefield and Heath, 1979). There from a swollen central body. Conidia ofremark- is also some resemblance at one stage of devel- ably similar form have been descdbed for Cy- opment of H. pycnidioideum pore pl:ugs (Ftc- 2'l) renella elegans Gochenaur, a dikaryotic basidio- Io those of the simple-pored, auricularioid fun- mycetous anamorph (Gochenaur, 1981). All of grs, Helicobasidium mompa Tanaka, as i\lvs- these morphologically unusual propagules can be tmted by Bourett and Mclaughlin (1986, Fie. considered as adaptations for water dispersal. 2t). Heterogastridium blepharistoma has been col- Nuclear division was not studied in detail in lectedon various types ofdecaying plant material this investigation of H. pycnidioideum. How- and mushrooms; isolates lrom Louisiana were ever, interphase and prophase SPBS are illus- found on oak litter that regularly is washed about trated (Frcs. 19, 20) to document structuml sim- by heavy rain during thunderstorms. Although ilarities with those in IL mompa (Bourett and the circumstances under which ltre Heterogas- Mclaughlin, 1986). SPBS with discs are char- tridium slate develops are unknown to us at this acteristic of species of the Uredinales (Heath, time, dispesal of the basidiospores can be e1- 1980; O'Donnell and Mclaughlin, 1981; Hoch pected to be by water. and Staples, 1983! Bauer, 1987). Additional Hetercgastridium blepharistoma hyphae vrere studies of mitotic and meiotic nuclear divisions reported to have mostly binucleate compart- are required for a more subslanlial comparison ments and simple septa (Bandoni and Ober- ofSPB developmenlal stages in different hetero- winkler, 1981). Binucleate compartments have basidiomycetous taxa. also been seen in TEM studies. Clamps are in- The unique features of H. pycnidioideum cleat Onsnwnu

ly indicate separation of the taxon from other nov., a dikaryotic anam otph. Mycotaxok l3-. 267 - auricularioid fungi. The species cannot be ac- 277. commodated in any ofthe currently recognized Heath, B. 1980. Fungal mitosis, the siglificance of variations on a theme. Mycologia 72:229-250. families and orders of such fungi. Therefore, a Hoch, H. C,, end R. C. Staples. 1983. Ultmstructuml new family and order are proposed for this organization of the non-difercnliated uredospore species, as follows: germliDg of Uromyces phaseoli variety typica. MycologiaTS: 795-824. Höhnel, F. von, 1918. Fungi imperfecri. Beiträge Heterogastridiaceae Oberwinklerand Bauer, /am. zur Kenntnis derselben. lledwigia 6t 129-209. nov. Ingold, C. T. 1942. Aquadc Hyphomycetes of de- cdyinglilter. Trahs. Heterobasidiomycetes fructificationibus pycnidioi- Btit. Mycol- Soc. 251 3394 17. 1961. The deis, meiosporangiis stalked spore drop. Nei' Phytol. transverse septatis, Gasrercmy- 60: l8l-183. cetum modo basidiosporis non eiectis. Basidiosporae Littlefield, J., rnd M. C. Heath, 1979. Uhrastructure triangulares. Plerumque slatus anamorphosiurn in pyc- -. of Rüst Fungi. Acade,)üc Press. New York. nidiis praesens est. Ma an, L., P, W. Wenzel, and D. Geier. 1979. TYPUS FAMILIAE: äe I erogast ridium OberwinkJer Methoden der Mikrokultivierung. Wiss. P.id- et Bauer, opus ipsum. H. ag. Hochsch. "W. Ratke" Köhen3/19791149-154. Marvanovä, L., and R. J. Bandoni. 1987. Naiadella Heterogastridiales Oberwinkler and Bater, ord. fluitans get et sp. nov.: a conidial basidiomycete. nor. Myco lo gia 79 | 5'7 8-58 6. Mclaughlin, D. J. 1980. Ultrastructure ofrhe meta- Descdptio eadem familiae Heterogastridiacearum. basidL\rn of A ricularia fuscosuccinea. AmeL J. TYPUS ORDINIS: Heterogastridiaceae Oberwiük- BoL67: l196-1206. ler et Bauer, opus ipsum. Moore, R. T. 1978. Taxonomic significance ofseptal ultrastructure with particular reference to jelly fun- gi. Mycologia 10:. 1007-1024. ACKNOWLEDGMENTS N.g Rqi, T. R. 1978. Genera Coelomycetum. XVI. Fibulocoela form-gen. nov., a coelomycete with We lhank Dr. C. T. Rogerson aDd Dr. Tatsuo yo- -lhe basidiomycetous amri lies. Canad. J. BoL 56:. 1485- koyama for providing i solates of H. blep haistoma. 1491. skilful technical assistance of Mrs. Angela Quellmalz- 1980. GeDera Coelomycetum xylll. Ellula Benz and Miss Sabine Süssbrich in TEM portions of anamorph-gen. nov., another coelomycete with this study is glatefully acknowledged. junior The au- -. basidiomycetous affiniti.es. Canad. J. Bot. 5812007 - thor also acknowledges with thanks the hospitality of 20r4. Dr. Arthur L. Welden and Tulane University for pro- Oberwinkler, F, 1985. Anmerkungen zur Evolution viding space and facililies where some aspects of the und Systematik der Basidiomyceten. Bot. Jahfi. study were originally carried out. Syst. 107:541-580. and R. J. Bandoni, 1982a. A laxonomic sur- vey of the gasteroid, auricularioid Heterobasidio- LITERATURE CTTED -, fiycetes. Canad. J. Bot.601 1726-l'750. and 1982b. Atractogloea: new genß Bandoni, R. 1972. Terreslrial occurrence of some J. Hoehnelomycetaceae (Heterobasidiomy- aquatic hyphomyceres. in the Canad. J. Bot. 50 2283- gia 2288. -t cetes). Myco-. lo 7 4t 634439. and F. Oberwinkler. 1981. Hyalopycnis O'Donnell, K. L,, and D. J. Mclaughlin. 1981. Ul- tmstructure meiosis the b lep ha ri st o m at a py cnidial basidiomycete. Candd. of in hollyhock rust fun- -t J. Bot.59: 1613-1620. grJs, Puccinia mall)acearum I. Prophase I-pro- and K. Tubaki. 1985. Cladoconidiumt a new fiet^phase l, Ptotoplasma 108. 225-244. hyphomycete anamorph genus. Trans. Japanese Patton,,4.., and R. Marchant. 1978. A marhematical -, Mycol. Soc. 26 425431. analysis of the dolipore/parenthesome stnrcture in Bauer, R. I 987. Uredinales-germination of basid- Basidiomycetes. "/. Gen. Mictobiol. 109. 335-349. iospores and pycnosporcs. Stud- in Mycology 30]. Petch, T, 1943. British Nect oideae and allied gen- 1l 1-125. efi' Truhs. Btit. Mycol. Soc.26i 53-70. Bouett, T. M, and D. J. Mclaughlin. 1986. Mitosis Porter, D., and W, F. Farnham. 1986. Mycaureola and septum formation in the basidiomycete llel- dilseae, a mali,neba,sidiomycele parasite ofthe red icobasidium nompa. Canad. J- Bot.64t 130-145. al9a, Dilsea carhosa. Trans. Brit- Mycol. Soc. 87.. Doguet, G. 1962. Digitatispora marina, n gen., n.sp., 5'.75-582. basidiomycöte marin. C. R. Hedb. S4ances Acad. Reynolds, E. S. 1963. The use oflead citrate at high Sci. Paris 254: 43364338. pH as an electrcn opaque stain in electron mi- 1967. Nia yibrissaMoore & Meyers, rema!- croscopy. ./. Ce Biol.lT: 208)12. quable basidiomycö1e main. C. R. Hedb. Seances Sebald, R. R. 1977. Feinstrukturstudien zur Onlo- -. Acad. Sci. Paris 265:. 1780-1783. genie von Arten der Urcdinales und verwandter Gochenaur, S, E. 1981. Ctyefiella elegans gen. et sp. Basidiomyceten. Thesis, Univ. Tübingen. 58 MYcorocrA

Seeler, E. V. 1943. Several fungicolous fu[gi. aar- Tübeki, K. 1969. Descriptive catalogue of I. F. O. lowia t ll9-133. fungus collection. lnn. Rep. Inst. Fennentatiok, SDürr,A.R. 1969. A low-viscosity epoxy embedding Osaka 4t 6U68. medium for electron microscopy. , Ultrastt. Res. 26.3143. Accepted for publication Augusl 16, 1989 Tu, C. C., rnd J. W. Kimbroügh, 1978. Systematics afld phylogeny of funpj in the Rhizocto ia cofr- plex. Bot. Gaz. 1391 45U66.