gjaerumia, a new genus in the georgefischeriales (ustilaginomycetes)

Gjaerumia, a new genus in the Georgefischeriales(Ustilaginomycetes)*

Robert BAUER, Matthias LUTZ and Franz OBERWINKLER

Universitat Tubingen, Botanisches Institut, Lehrstuhl Spezielle Botanik und Mykologie, Auf der Morgenstelle 1,D-72076 Tubingen, Germany.E-mail : [email protected]

Received 26 April 2005; accepted 1 July 2005.

Teliospores, basidia, cultures, hyphal septations, cellular interactions and nucleotide sequences from the D1/D2 region of

the nuclear large subunit ribosomal RNA gene of Entyloma ossifragi occurring on Narthecium ossifragum (Nartheciaceae)were examined and compared with findings in the Georgefischeriales and other Ustilaginomycetes. The data showthat Entyloma ossifragi is a member of the Georgefischeriales. Among the Georgefischeriales, Entyloma ossifragi

morphologically is very similar to Jamesdicksonia species, but differs from this genus and all other Georgefischerialesby the formation of dolipores without striations that become closed during teliosporogenesis. In addition, in ourmolecular phylogenetic analyses Entyloma ossifragi stands well apart from Jamesdicksonia, forming with some Tilletiopsis

specimens a statistically supported cluster. Accordingly, the genus Gjaerumia gen. nov. and the family Gjaerumiaceaefam. nov. are proposed to accommodate Entyloma ossifragi in the Georgefischeriales. The new combination G. ossifragi(syn. Entyloma ossifragi) is made.

INTRODUCTION

In the new system of Ustilaginomycetes, the orderGeorgefischeriales was erected for species havinglocal interaction zones and poreless septa at maturity(Bauer, Oberwinkler & Vanky 1997). Haustoria orother intracellular fungal organs are lacking. MostGeorgefischeriales occur on grasses and they generallysporulate in vegetative parts of their respective hosts.The teliospore masses are usually not powdery andwith a few exceptions the sori are not exposed by rup-ture of the host tissues. Molecular analyses confirmedthis group (Begerow, Bauer & Oberwinkler 1997).

Bauer et al. (2001a) discussed the phylogeny of theGeorgefischeriales, resulting in the division of thisgroup into the three families Eballistraceae, George-fischeriaceae and Tilletiariaceae, whereas the ana-morphic Tilletiopsis minor was considered as arepresentative of a fourth group of the order. TheTilletiariaceae are phragmobasidiate, whereas theEballistraceae and the Georgefischeriaceae are holo-basidiate. The Eballistraceae differ from the George-fischeriaceae and Tilletiariaceae in the lack of theballistospore mechanism. This study also revealed that

the genus Entyloma is polyphyletic and that dark-coloured Entyloma species occurring on monocotsbelong to the Georgefischeriales. In addition, in thisstudy a dilemma in Georgefischeriales systematicsbecame evident : morphology of sori and teliosporesalone is unsufficient to ascribe candidates for theGeorgefischeriales to any of the taxa of this group.

One of the existing candidates for the Georgefischer-iales is Entyloma ossifragi occurring on Nartheciumossifragum (Nartheciaceae ; e.g. Tamura et al. 2004).Our preliminary ultrastructural studies using driedreference material suggested that the fungus was amember of the Georgefischeriales. However, as dis-cussed above, data concerning basidial morphology,culture characteristics and (or) DNA sequences arenecessary to ascribe Entyloma ossifragi to any of thegenera and families of the Georgefischeriales. There-fore, we repeatedly attempted to collect fresh materialof this fungus in Germany, Denmark, and Sweden, butwithout success. In Sweden, we unsuccessfully searchedthrough several tremendous Narthecium populationsin Smaland and Vastergotland where the fungus wascollected at the beginning of the 20th century. Even inthe type location in Silkeborg Vesterskov, Denmark,where on 17 Sept. 1885 E. Rostrup found the fungus,we detected only a few individuals of Narthecium

* Part 225 in the series Studies in Heterobasidiomycetes from theBotanical Institute, University of Tubingen.

Mycol. Res. 109 (11): 1250–1258 (November 2005). f The British Mycological Society 1250

doi:10.1017/S0953756205003783 Printed in the United Kingdom.

ossifragum. However, during the 7th InternationalMycological Congress 2002 in Oslo we met theNorwegian mycologist Halvor B. Gjaerum, who hadcollected E. ossifragi in 1969. As a result of thisget-together, we were able to recollect the fungus.Subsequently, the Norwegian biologist Ivar Mysterudfound the fungus in numerous places in Norway. Here,we discuss the characteristics of this plant parasite.

MATERIALS AND METHODS

The following collections were used:

Eballistra lineata (syn. Entyloma lineatum) on Zizania aqua-tica var. angustifolia : Canada : Manitoba : Lake Winnipeg,

Delta of Bradbury River, 22 Aug. 1989, B., B. & J. Nielsen(K. Vanky: Ust. 741). – Gjaerumia ossifragi (syn. Entylomaossifragi) on Narthecium ossifragum : Norway : Møre ogRomsdal, Molde, Skaret, 14 Aug. 2002, R. Bauer & M. Lutz

(M 0098772, TUB 011637).

Basidia were obtained from teliospores spread thinlyon water agar and malt-yeast-peptone agar (Bandoni1972) in Petri dishes at ca 20 xC. Cultures were grownon malt yeast peptone agar.

The ultrastructure of septa, cellular interactions andteliospore walls were studied with a Zeiss EM 109transmission electron microscope at 80 kV. Sampleswere fixed overnight with 2% glutaraldehyde in 0.1 M

sodium cacodylate buffer (pH 7.2) at room tempera-ture. Following six transfers in 0.1 M sodium cacodylatebuffer, samples were postfixed in 1% osmium tetroxidein the same buffer for 1 h in the dark, washed in dis-tilled water, and stained in 1% aqueous uranyl acetatefor 1 h in the dark. After five washes in distilled water,samples were dehydrated in acetone, using 10 minchanges at 25%, 50%, 70%, 95%, and three timesin 100% acetone. Samples were embedded in Spurr’splastic and sectioned with a diamond knife. Serial sec-tions were mounted on formvar-coated, single-slotcopper grids, stained with lead citrate at room tem-perature for 5 min, and washed with distilled water.

Genomic DNA was isolated from Eballistra lineataand Gjaerumia ossifragi (syn. Entyloma ossifragi). Formethods of isolation and crushing of fungal material,DNA extraction, amplification, purification of PCRproducts, sequencing, and processing of the raw datasee Lutz et al. (2004). The 5k-end (about 625 bp) ofthe nuclear large subunit ribosomal DNA (nuc-LSUrDNA), comprising the domains D1 and D2 (Guadetet al. 1989), was amplified using the primer pair NL1and NL4 (O’Donnell 1992, 1993). DNA sequencesdetermined for this study were deposited in GenBank,GenBank accession number are AY525372 (Eballistralineata) and AY525373 (Gjaerumia ossifragi).

To obtain a hypothesis on the phylogenetical pos-ition of Gjaerumia ossifragi (syn. Entyloma ossifragi),we analysed a data set containing the sequenceof Gjaerumia ossifragi and all sequences of speciesbelonging to the Eballistraceae, Georgefischeriaceae,

Gjaerumiaceae and Tilletiariaceae of the George-fischeriales available at GenBank (http://www.ncbi.nlm.nih.gov) (with the exception of the sequence ofEballistra lineata AF229351, which was much shorterthan our sequences ; therefore we sequenced anotherspecimen of the species) together with an assortmentof species covering most of the orders of Ustilagino-mycetes (taxonomical concept after Bauer et al.(2001a) (GenBank accession numbers are given inparentheses) :

Doassansia epilobii (AF007523), Doassinga callitrichis (syn.Entyloma callitrichis) (AF007525), Eballistra brachiariae (syn.Melanotaenium brachiariae) (AF009864), Eballistra oryzae

(syn. Entyloma oryzae) (AF229353), Entyloma atlanticum(AY081011), Entyloma calendulae (AY081012), Entylomaficariae (AY081013), Erratomyces patelii (AF009855),

Exobasidium vaccinii (AF009858), Georgefischeria riveae(AF009861), Graphiola phoenicis (AF009862), Ingoldiomyceshyalosporus (AF133576), Jamesdicksonia brunkii (syn.Tolyposporella brunkii) (AF009875), Jamesdicksonia dacty-

lidis (syn. Entyloma dactylidis) (AF009853), Jamesdicksoniairregularis (syn. Entyloma irregulare) (AF229352), James-dicksonia ischaemiana (syn. Melanotaenium ischaemianum)

(AF229355),Microstroma juglandis (AF009867),Nannfeldtio-myces sparganii (AF007527), Phragmotaenium indicum(syn. Melanotaenium indicum) (AF229354), Rhamphospora

nymphaeae (AF007526), Tilletia caries (AJ235307), Tilletiariaanomala (AJ235284), Tilletiopsis derxii (AB052823), Tille-tiopsis flava (AJ235285), Tilletiopsis fulvescens 244/607.83

(AJ235281/AJ235282), Tilletiopsis minor 543.50/111.629(AJ235287/AY272012), Tilletiopsis oryzicola (AB052824),Tilletiopsis penniseti (AB052825), Tilletiopsis sp. 26212/247.52(AF459717/AJ235288), Tilletiopsis washingtonensis 435.92/

605.83 (AJ235309/AJ235279), Ustilago avenae (AJ236140),Ustilago nuda (AJ236139), Ustilago scitaminea (AJ236138),Ustilago trichophora (AJ236141), Volvocisporium triumfetti-

cola (syn. Muribasidiospora triumfetticola) (AF352053).

Following the argumentation of Lee (2001), weused a multiple analysis approach to sequence align-ment as modified by Markus Goker (pers. comm.). Toget reproducible results, we avoided both manipulationof alignments by hand and manual exclusion of anypositions. To align sequences, we used three align-ment algorithms, POA (Lee, Grasso & Sharlow 2002),CHAOS 0.931/DIALIGN 2.2.1 (Morgenstern 1999,Brudno et al. 2003), and MAFFT 3.85 (Katoh et al.2002), which were shown by simulation and empiricalstudies to be quite accurate (Katoh et al. 2002,Lassmann & Sonnhammer 2002).

To estimate phylogenetic relationships, we applied aBayesian approach of phylogenetic inference usinga Markov chain Monte Carlo (MCMC) technique asimplemented in the computer program MrBayes 3.0B4(Huelsenbeck & Ronquist 2001) to each of the threealignments independently. For bayesian analysis, eachalignment was first analysed with MrModeltest 1.0b(Johan A. A. Nylander, Uppsala University, Sweden;Posada & Crandall 1998) to find the most appropriatemodel of DNA substitution (Lemmon & Moriarty2004). The hierarchical likelihood ratio test suggested

R. Bauer, M. Lutz and F. Oberwinkler 1251

the DNA substitution model GTR+I+G forthe MAFFT and POA alignment, respectively, andSYM+I+G for the DIALIGN alignment; Swoffordet al. (1996) survey the various DNA substitutionmodels. Thus, for each alignment, four incrementallyheated simultaneous Markov chains were run over 2 Mgenerations using random starting trees and defaultstarting parameters of the respective DNA substitutionmodel (Huelsenbeck & Ronquist 2001). Trees weresampled every 100th generation resulting in an overallsampling of 20 001 trees for each alignment. Fromthese, the first 1001 trees were discarded (burnin=1001). A 50% majority-rule consensus tree wascomputed from the combined set of trees (27 000 trees)sampled after the process had reached stationarityin the three independent runs based on the differentalignments, the rationale being that only clades thatwere well-supported in trees inferred from all align-ments could approximately be regarded as supportedindependently of ambiguities in alignment solutions.This Bayesian approach of phylogenetic analysis wasrepeated five times to test the independence of theresults from topological priors (Huelsenbeck et al.2002). Patristic distance matrices for all 27 000 treesas well as the mean of these matrices (Lapointe &Cucumel 1997) were computed using a PERL scriptwritten by Clemens Oertel (available on request). Themean distance matrix was used to estimate branchlengths of the majority-rule consensus tree usingPAUP* version 4.0b10 (Swofford 2001).

RESULTS

Teliospores, hyphal septation and cellular interaction

Teliospores were developed in the intercellular spacesin the mesophyll. The mass of sporogenous hyphaewas usually completely used for teliospore formation.The teliospore wall consisted of an electron-opaqueexosporium (terminology follows Piepenbring, Bauer& Oberwinkler 1998), occasionally covered by rem-nants of the sheath and the wall of the sporogenoushypha, and an electron-transparent endosporium(Figs 1–2, layers labelled in Fig. 2). In young telio-spores the endosporium may be lacking. Teliosporeswere smooth.

Maturing soral hyphae had dolipores (Fig. 3).Dolipores were simple, lacking associated cisternaeand any striation in the pore. During teliosporogenesis,the pores become closed (not illustrated).

Cellular interactions were discussed in detail byBauer et al. (1997) and are therefore only briefly sum-marized here. The soral mycelium in Entyloma ossifragiwas only intercellular, lacking haustoria or intracellularhyphae. However, local interaction zones with smallelectron-opaque deposits of variable shape were pres-ent in intercellular hyphae attached to the host cells(Fig. 4). Only the host response at these sites indicatedthat they were sites of interaction.

Basidia

Teliospore germination resulted in holobasidia withterminal basidiospores in Entyloma ossifragi (Figs 5–6,9–12). Basidia were variable in form: in long basidiausually retraction septa were formed. Basidiosporeswere more or less symmetrical and fusiform and werepassively released. Occasionally, but not always, theyconjugated on the basidium (Fig. 11). The conjugatedbasidiospores germinated apically or laterally while stillconnected to the basidium, producing ballistoconidia(Fig. 11). However, unconjugated basidiospores, whilestill connected to the basidium, occasionally alsoformed ballistoconidia (Fig. 12).

Cultural characteristics

Two different cultural growth forms were found. Ingeneral after discharge, the ballistic propagules becametwo-celled with a transverse septum and began togerminate at both poles (Fig. 13). Subsequently, onone side a Tilletiopsis-culture generating pseudomyceliawith retraction septa and ballistoconidia appeared(Fig. 7), while on the other side true mycelia generatingteliospores developed (Figs 8, 14). Teliospores in thecultures germinated in an identical way to those formedby the soral hyphae.

Molecular phylogenetic analyses

In our molecular phylogenetic analyses using partialnuclear large subunit ribosomal DNA sequences,Entyloma ossifragi was tested together with all knowngeorgefischeriaceous sequences, at least two rep-resentatives of all orders of the Exobasidiomycetidae,and some Ustilago species (Fig. 15). Using the Ustilagospecies as outgroup, the statistically well-supportedgroups appearing in the Bayesian phylogenetic treewere congruent to the orders discussed by Bauer et al.(1997, 2001b). In addition, the members of theGeorgefischeriales were grouped in the expectedfamilies : the monophyly of the Tilletiariaceae andEballistraceae was supported by a 100% a posterioriprobability, respectively. Although the group rep-resenting the Georgefischeriaceae appeared in a poly-tomy, our molecular phylogenetic analysis can notreject the hypothesis of the monophyly of theGeorgefischeriaceae. E. ossifragi appeared on a com-mon branch with the Eballistraceae, whereat its se-quence showed the highest similararity to the sequencesof Tilletiopsis minor, T. penniseti and some otherTilletiopsis strains, compared to the sequence dataavailable in GenBank.

DISCUSSION

Gjaerumia and Gjaerumiaceae

Our molecular phylogenetic analyses demonstratethat Entyloma ossifragi is a member of the

Gjaerumia gen. nov. (Georgefischeriales) 1252

Georgefischeriales. This phylogenetic hypothesis agreeswell with the ultrastructural data. As in the otherGeorgefischeriales (Bauer et al. 1997, 2001a, b), E. ossi-fragi grows only intercellularly, interacts with itshost by the formation of local interaction zones, andhas no pores in mature soral septa. Interestingly,

E. ossifragi, like Tilletiaria anomala (Bandoni & Johri1972), forms teliospores and basidia in culture.Morphologically, however, E. ossifragi is very similarto species of Jamesdicksonia and we do not know ofa morphological criterion that distinguishes E. ossi-fragi from Jamesdicksonia. Thus, E. ossifragi shares

Figs 1–4. Ultrastructure of Gjaerumia ossifragi (syn. Entyloma ossifragi). Fig. 1. Section through a sporogenous hyphashowing the formation of a teliospore. Note that the teliospore is surrounded by the wall of the sporogenous hypha.Fig. 2. Teliospore wall in detail with sheath (arrowhead), exosporium (small arrow) and endosporium (large arrow).

Fig. 3. Dolipore in a young soral hypha. Fig. 4. Intercellular hypha (ih) of G. ossifragi in contact with host cell wall (HW)showing an interaction site with a small deposit (arrow). Host response to infection is visible at R. Bars: Fig. 1=1 mm,Fig. 2=0.5 mm; and Figs 3–4=0.2 mm.


the formation of holobasidia with ballistosporic pro-pagules and the Tilletiopsis-growth in culture withJamesdicksonia (Bauer et al. 2001a). However, E. ossi-fragi differs from Jamesdicksonia and all otherGeorgefischeriales in its parasitism on a member ofthe Nartheciaceae (e.g. Tamura et al. 2004) and inthe formation of dolipores in maturing soral hyphae.

These differences clearly separate E. ossifragi fromJamesdicksonia and the other Georgefischeriales. Thisphylogenetic indication essentially agrees with themolecular results. E. ossifragi forms, with Tilletiopsisminor, T. penniseti and some other Tilletiopsis strains,a statistically supported clade, well separated fromJamesdicksonia. This clade appears on a common

Figs 5–8. Phase contrast micrographs of Gjaerumia ossifragi (syn. Entyloma ossifragi). Figs 5–6. Two basidia. Note thevariable shape of the basidia. Fig. 7. Tilletiopsis-growth in culture. Ballistoconidia are visible at b. Fig. 8. Teliospore

formation in culture. Bars=10 mm.


branch with representatives of the Eballistraceaewith an a posteriori probability of 82%. However, themembers in the E. ossifragi clade form ballistosporicpropagules and have a Tilletiopsis-anamorph, whereasthose of the Eballistraceae lack the ballistosporemechanism and form instead a budding yeast phase.These differences clearly separate the E. ossifragi cladefrom the Eballistraceae. Accordingly, a new family andgenus are necessary to accommodate E. ossifragi in theGeorgefischeriales.

As the other Georgefischeriales, the septa in thesoral hyphae in Gjaerumia are poreless at maturity. In

contrast with the other Georgefischeriales, however,during the septation process Gjaerumia forms regulardolipores. In the other Georgefischeriales, in youngsepta poroid structures are sometimes visible, but noregular pores (Bauer et al. 1997). It is evident from thisstudy that in Gjaerumia the septa close later duringmaturation than in the other Georgefischeriales. Be-cause in the Exobasidiomycetidae poreless septa occuronly in the Georgefischeriales, we consider the loss ofseptal pores as apomorphic for the Georgefischeriales.Accordingly, Gjaerumia may occupy a systematicposition at the base of the Georgefischeriales. This

9

10

11

12

14

13

b

b

b

Figs 9–14. Line drawings of Gjaerumia ossifragi (syn. Entyloma ossifragi). Figs 9–12. Basidia of variable shape.Ballistoconidia are visible at b; note the conjugation of the basidiospores in Fig. 11. Fig. 13. Germination of

ballistoconidia; note the internal septation of the ballistoconidia. Fig. 14. Teliospore formation in culture. Bar=10 mm.


phylogenetic indication is not in conflict with the resultof the molecular analyses.

The formation of dolipores in maturing soral hyphaeof Gjaerumia may also reflect that the George-fischeriales arose from a doliporic ancestor. Within theExobasidiomycetidae, the Tilletiales also form dolipores(Bauer et al. 1997) and have some features in commonwith the Georgefischeriales : the members of both

groups grow only intercellularly and they form localinteraction zones without interaction apparatus (Baueret al. 1997, 2001b). In addition, the Tilletiales as wellas the Georgefischeriales live predominantly on grasses.In contrast with Gjaerumia, the pore channels in theTilletiales are striated (Bauer et al. 1997, 2001b). Any-way, it is quite possible that the dolipores occurringin the Tilletiales and in Gjaerumia are homologous,

Fig. 15. Bayesian inference of phylogenetic relationships within the Exobasidiomycetidae : Majority rule consensus treefrom 27 000 trees that were obtained by three independent Monte Carlo Markov chain analysis of three alignmentscomputed with MAFFT, POA and DIALIGN of nuc-LSU rDNA sequences using the GTR+I+G (MAFFT, POA

alignment) and SYM+I+G (DIALIGN alignment) model of DNA substitution, random starting trees and default startingparameters of the substitution. The topology was rooted with Ustilago avenae, U. nuda, U. tricophora, and U. scitaminea(Ustilaginomycetidae). Numbers on branches are estimates for a posteriori probabilities. Patristic distance matrices for all27 000 trees as well as the mean of these matrices (Lapointe & Cucumel 1997) were computed and used to estimate branch

lengths of the majority-rule consensus. They are scaled in terms of expected numbers of nucleotide substitutions per site.The taxonomical concept applied corresponds to Bauer et al. (2001a, b).


reflecting a common evolutionary origin of the George-fischeriales and Tilletiales.

Within the Ustilaginomycetes, the species of Ento-rrhiza also form dolipores. As in Gjaerumia, the doli-pores in Entorrhiza lack any striation. Morphologicallyand ecologically, however, Entorrhiza differs sig-nificantly from the Tilletiales and Georgefischeriales.Thus, species of Entorrhiza form teliospores in livinghost cells (Fineran 1980), they produce galls on rootsof Juncaceae and Cyperaceae, and the teliosporesgerminate internally by becoming four-celled duringgermination (Bauer et al. 2001b, Fineran 1982).Obviously, dolipores evolved at least twice in theustilaginomycetous phylogeny, i.e., in the phylogeniesof Entorrhizomycetidae and Exobasidiomycetidae.

TAXONOMY

Gjaerumiaceae R. Bauer, M. Lutz & Oberw., fam. nov.

Fungi Georgefischerialium sensu Bauer et al. (1997) doliporisin hyphis iuvenibus parasiticis. Status anamorphosium ingenus Tilletiopsis Derx pertinet.

Typus : Gjaerumia R. Bauer, M. Lutz & Oberw. 2005.

Members of the Georgefischeriales sensu Bauer et al.(1997) having dolipores in young parasitic hyphae.Anamorph classified in the form genus Tilletiopsis.

Gjaerumia R. Bauer, M. Lutz & Oberw., gen. nov.

Etym. : Referring to the Norwegian mycologistHalvor B. Gjaerum, who gave us a detailed descriptionof the place where he found the fungus in 1969.

Fungi Georgefischerialium sensu Bauer et al. (1997) doliporisin hyphis iuvenibus parasiticis. Parasitantur in Nartheciaceis.Typus : Gjaerumia ossifragi (Rostr.) R. Bauer, M. Lutz &

Oberw. 2005.

Members of the Georgefischeriales sensu Bauer et al.(1997) having dolipores in young parasitic hyphae.Parasitic on Nartheciaceae.

Gjaerumia ossifragi (Rostr.) R. Bauer, M. Lutz &Oberw., comb. nov.

Basionym: Entyloma ossifragi Rostr., Festskr. Bot.Foren. Kjøbenhavn 1890 : 133 (1890).

ACKNOWLEDGEMENTS

We thank Halvor B. Gjaerum for his help to collect the fungus,

Michael Weiß for critically reading the manuscript and for provid-

ing the Latin diagnoses, Magda Wagner-Eha, Jaqueline Gotze

and Friedhelm Albrecht for technical assistance, and the Deutsche

Forschungsgemeinschaft for financial support.

REFERENCES

Bandoni, R. J. (1972) Terrestrial occurrence of some aquatic

hyphomycetes. Canadian Journal of Botany 50 : 2283–2288.

Bandoni, R. J. & Johri, B. N. (1972) Tilletiaria : a new genus in the

Ustilaginales. Canadian Journal of Botany 50 : 39–43.

Bauer, R., Oberwinkler, F. & Vanky, K. (1997) Ultrastructural

markers and systematics in smut fungi and allied taxa. Canadian

Journal of Botany 75 : 1273–1314.

Bauer, R., Begerow, D., Nagler, A. & Oberwinkler, F. (2001a)

The Georgefischeriales : a phylogenetic hypothesis. Mycological

Research 105 : 416–424.

Bauer, R., Begerow, D., Oberwinkler, F., Piepenbring, M. &

Berbee, M. L. (2001b) Ustilaginomycetes. In The Mycota. Vol. 7B.

Systematics and evolution (D. J. McLaughlin, E. G. McLaughlin &

P. A. Lemke, eds): 57–83. Springer-Verlag, Berlin.

Begerow, D., Bauer, R. & Oberwinkler, F. (1997) Phylogenetic

studies on nuclear large subunit ribosomal DNA sequences of

smut fungi and related taxa. Canadian Journal of Botany 75 :

2045–2056.

Brudno, M., Chapman, M., Gottgens, B., Batzoglou, S. &

Morgenstern, B. (2003) Fast and sensitive multiple alignment

of large genomic sequences. BMC Bioinformatics 4 : 66.

Fineran, J. M. (1980) The structure of galls induced by Entorrhiza C.

Weber (Ustilaginales) on roots of the Cyperaceae and Juncaceae.

Nova Hedwigia 32 : 265–284.

Fineran, J. M. (1982) Teliospore germination in Entorrhiza caspar-

yana (Ustilaginales). Canadian Journal of Botany 60 : 2903–2913.

Guadet, J., Julien, J., Lafay, J. F. & Brygoo, Y. (1989) Phylogeny

of some Fusarium species, as determined by large-subunit rRNA

sequence comparison.Molecular Biology and Evolution 6 : 227–242.

Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian

inference of phylogenetic trees. Bioinformatics Applications Note

17 : 754–755.

Huelsenbeck, J. P., Larget, B., Miller, R. E. & Ronquist, F. (2002)

Potential applications and pitfalls of Bayesian inference of

phylogeny. Systematic Biolology 51 : 673–688.

Key to the families and genera of Georgefischeriales

1 On Nartheciaceae (Gjaerumiaceae) ; dolipores present in young parasitic hyphae . . . . . Gjaerumia

On other hosts ; dolipores absent in young parasitic hyphae . . . . . . . . . . 2

2(1) Phragmobasidia present (Tilletiariaceae) . . . . . . . . . . . . . 3Holobasidia present . . . . . . . . . . . . . . . . . 5

3(2) Teliospores echinulate . . . . . . . . . . . . . . . Tilletiaria

Teliospores smooth . . . . . . . . . . . . . . . . . 4

4(3) Single teliospores . . . . . . . . . . . . . . PhragmotaeniumSporeballs . . . . . . . . . . . . . . . . . Tolyposporella

5(2) Ballistosporic propagules absent (Eballistraceae) . . . . . . . . . . . Eballistra

Ballistosporic propagules present (Georgefischeriaceae) . . . . . . . . . . 6

6(5) Teliospores lightly coloured . . . . . . . . . . . . . Georgefischeria

Teliospores darkly pigmented . . . . . . . . . . . . . Jamesdicksonia


Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a

novel method for rapid multiple sequence alignment based on fast

Fourier transform. Nucleic Acids Research 30 : 3059–3066.

Lapointe, F.-J. & Cucumel, G. (1997) The average consensus

procedure: combination of weighted trees containing identical

or overlapping sets of taxa. Systematic Biology 46 : 306–312.

Lassmann, T. & Sonnhammer, E. L. L. (2002) Quality assessment

of multiple alignment programs. FEBS Letters 529 : 126–130.

Lee, M. S. Y. (2001) Unalignable sequences and molecular evolution.

Trends in Ecology & Evolution 16 : 681–685.

Lee, C., Grasso, C. & Sharlow, M. (2002) Multiple sequence align-

ment using partial order graphs. Bioinformatics 18 : 452–464.

Lemmon, A. R. & Moriarty, E. C. (2004) The importance of proper

model assumption in Bayesian phylogenetics. Systematic Biology

53 : 265–277.

Lutz, M., Bauer, R., Begerow, D., Oberwinkler, F. & Triebel, D.

(2004) Tuberculina : rust relatives attack rusts. Mycologia 96 :

614–626.

Morgenstern, B. (1999) DIALIGN 2: improvment of the segment-

to-segent approach to multiple sequence alignment. Bioinformatics

15 : 211–218.

O’Donnell, K. L. (1992) Ribosomal DNA internal transcribed

spacers are highly divergent in the phytopathogenic ascomycete

Fusarium sambucinum (Gibberella pulicaris). Current Genetics 22 :

213–220.

O’Donnell, K. L. (1993) Fusarium and its near relatives. In The

Fungal Holomorph: mitotic, meiotic and pleomorphic speciation in

fungal systematics (D. R. Reynolds & J. W. Taylor, eds) : 225–233.

CAB International, Wallingford.

Piepenbring, M., Bauer, R. & Oberwinkler, F. (1998) Teliospores of

smut fungi. General aspects of teliospore walls and sporogenesis.

Protoplasma 204 : 155–169.

Posada, D. & Crandall, K. A. (1998) MODELTEST: testing the

model of DNA substitution. Bioinformatics 14 : 817–818.

Swofford, D. L. (2001) PAUP*: phylogenetic analysis using parsi-

mony (*and other methods). Version 4.0b10. Sinauer Associates,

Sunderland, MA.

Swofford, D. L., Olsen, G. J., Waddell, P. J. & Hillis, D. M. (1996)

Phylogenetic Inference. In Molecular Systematics (D. M. Hillis,

C. Moritz & B. K. Mable, eds) : 407–514. Sinauer Associates,

Sunderland, MA.

Tamura, M. N., Fuse, S., Azuma, H. & Hasebe, M. (2004)

Biosystematic studies on the family Tofieldiaceae I. Phylogeny and

circumscription of the family inferred from DNA sequence of

matK and rbsL. Plant Biology 6 : 562–567.

Corresponding Editor: S. Takamatsu


gjaerumia, a new genus in the georgefischeriales (ustilaginomycetes)

Documents